Autocrine/paracrine growth hormone in cancer progression

in Endocrine-Related Cancer
Authors:
Xi Zhang Shenzhen Bay Laboratory, Shenzhen, P R China

Search for other papers by Xi Zhang in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-4093-0897
,
Vijay Pandey Tsinghua Berkeley Shenzhen Institute and Institute of Biopharmaceutical and Health Engineering, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, P R China

Search for other papers by Vijay Pandey in
Current site
Google Scholar
PubMed
Close
,
Vipul Bhardwaj Tsinghua Berkeley Shenzhen Institute and Institute of Biopharmaceutical and Health Engineering, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, P R China

Search for other papers by Vipul Bhardwaj in
Current site
Google Scholar
PubMed
Close
,
Tao Zhu Shenzhen Bay Laboratory, Shenzhen, P R China
Department of Oncology, The First Affiliated Hospital of USTC, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, P R China
The CAS Key Laboratory of Innate Immunity and Chronic Disease, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, Anhui, P R China

Search for other papers by Tao Zhu in
Current site
Google Scholar
PubMed
Close
, and
Peter E Lobie Shenzhen Bay Laboratory, Shenzhen, P R China
Tsinghua Berkeley Shenzhen Institute and Institute of Biopharmaceutical and Health Engineering, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, P R China

Search for other papers by Peter E Lobie in
Current site
Google Scholar
PubMed
Close

Correspondence should be addressed to P E Lobie: pelobie@sz.tsinghua.edu.cn

*(X Zhang and V Pandey contributed equally to this work)

This paper is part of a themed collection on the role of Growth Hormone in Endocrine Cancers. The Guest Editor for this collection was John Kopchick, Ohio University, USA.

Restricted access
Rent on DeepDyve

Sign up for journal news

Abstract

It is now apparent that growth hormone (GH), an anterior pituitary hormone predominantly regulating postnatal somatic growth and metabolism, is also expressed in extrapituitary tissues. An extrapituitary synthetic site of GH that has garnered interest is the de novo or enhanced expression of GH in carcinoma or other cancers. In a number of cancers, including carcinoma of the mammary gland, endometrium, liver, prostate, and colon, the expression of GH is independently associated with more advanced clinicopathologic parameters of the cancer. In some of these cancers, tumor human growth hormone (hGH) expression portends worse survival outcomes for patients. Functionally, tumor-derived hGH exerts both autocrine and paracrine functions on carcinoma cells and cancer-associated stroma. Expression of autocrine/paracrine hGH in cancer drives tumor growth, angiogenesis, metastasis, and resistance to therapy by promotion of cancer cell proliferation, survival, epithelial-to-mesenchymal transition, motility, invasion, cancer stem cell-like behavior, and metastasis. Autocrine/paracrine hGH activates oncogenic signaling pathways and specific transcriptome signatures and enhances the expression of an oncogenic secretome to promote these functions. Hence, extrapituitary expression of GH in cancer promotes cancer progression independent of endocrine hGH, and may be considered as a validated target in oncology.

 

  • Collapse
  • Expand
  • Álvarez-Garcia V, Tawil Y, Wise HM & & Leslie NR 2019 Mechanisms of PTEN loss in cancer: it’s all about diversity. Seminars in Cancer Biology 59 6679. (https://doi.org/10.1016/j.semcancer.2019.02.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Baskari S, Govatati S, Madhuri V, Nallabelli N, K PM, Naik S, Poornachandar, Balka S, Tamanam RR & & Devi VR 2017 Influence of autocrine growth hormone on NF-κB activation leading to epithelial-mesenchymal transition of mammary carcinoma. Tumour Biology 39 1010428317719121. (https://doi.org/10.1177/1010428317719121)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bougen NM, Yang T, Chen H, Lobie PE & & Perry JK 2011 Autocrine human growth hormone reduces mammary and endometrial carcinoma cell sensitivity to mitomycin C. Oncology Reports 26 487493. (https://doi.org/10.3892/or.2011.1305)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bougen NM, Steiner M, Pertziger M, Banerjee A, Brunet-Dunand SE, Zhu T, Lobie PE & & Perry JK 2012 Autocrine human GH promotes radioresistance in mammary and endometrial carcinoma cells. Endocrine-Related Cancer 19 625644. (https://doi.org/10.1530/ERC-12-0042)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Brittain AL, Basu R, Qian Y & & Kopchick JJ 2017 Growth hormone and the epithelial-to-mesenchymal transition. Journal of Clinical Endocrinology and Metabolism 102 36623673. (https://doi.org/10.1210/jc.2017-01000)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Brunet-Dunand SE, Vouyovitch C, Araneda S, Pandey V, Vidal LJ-P, Print C, Mertani HC, Lobie PE & & Perry JK 2009 Autocrine human growth hormone promotes tumor angiogenesis in mammary carcinoma. Endocrinology 150 13411352. (https://doi.org/10.1210/en.2008-0608)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Buckels A, Zhang Y, Jiang J, Athar M, Afaq F, Shevde-Samant L & & Frank SJ 2020 Autocrine/paracrine actions of growth hormone in human melanoma cell lines. Biochemistry and Biophysics Reports 21 100716. (https://doi.org/10.1016/j.bbrep.2019.100716)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cagnol S & & Rivard N 2013 Oncogenic KRAS and BRAF activation of the MEK/ERK signaling pathway promotes expression of dual-specificity phosphatase 4 (DUSP4/MKP2) resulting in nuclear ERK1/2 inhibition. Oncogene 32 564576. (https://doi.org/10.1038/onc.2012.88)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Carter-Su C, King AP, Argetsinger LS, Smit LS, Vanderkuur J & & Campbell GS 1996 Signalling pathway of GH. Endocrine Journal 43 (Supplement) S65S70. (https://doi.org/10.1507/endocrj.43.suppl_s65)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen RM, Chiou YS, Chong QY, Poh HM, Tan TZ, Zhang MY, Ma L, Zhu T, Pandey V & Basappa et al.2019 Pharmacological Inhibition of TFF3 Enhances Sensitivity of CMS4 Colorectal Carcinoma to 5-Fluorouracil through Inhibition of p44/42 MAPK. International Journal of Molecular Sciences 20 6215. (https://doi.org/10.3390/ijms20246215)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen YJ, You ML, Chong QY, Pandey V, Zhuang QS, Liu DX, Ma L, Zhu T & & Lobie PE 2017 Autocrine human growth hormone promotes invasive and cancer stem cell-like behavior of hepatocellular carcinoma cells by STAT3 dependent inhibition of CLAUDIN-1 expression. International Journal of Molecular Sciences 18 1274. (https://doi.org/10.3390/ijms18061274)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen YJ, Zhang X, Wu ZS, Wang JJ, Lau AY-C, Zhu T & & Lobie PE 2015 Autocrine human growth hormone stimulates the tumor initiating capacity and metastasis of estrogen receptor-negative mammary carcinoma cells. Cancer Letters 365 182189. (https://doi.org/10.1016/j.canlet.2015.05.031)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cheng F, Wang X, Chiou YS, He C, Guo H, Tan YQ, Basappa B, Zhu T, Pandey V & & Lobie PE 2022 Trefoil factor 3 promotes pancreatic carcinoma progression via WNT pathway activation mediated by enhanced WNT ligand expression. Cell Death and Disease 13 265. (https://doi.org/10.1038/s41419-022-04700-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chesnokova V & & Melmed S 2019 Growth hormone in the tumor microenvironment. Archives of Endocrinology and Metabolism 63 568575. (https://doi.org/10.20945/2359-3997000000186)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chesnokova V, Zonis S, Apostolou A, Estrada HQ, Knott S, Wawrowsky K, Michelsen K, Ben-Shlomo A, Barrett R & Gorbunova V et al.2021 Local non-pituitary growth hormone is induced with aging and facilitates epithelial damage. Cell Reports 37 110068. (https://doi.org/10.1016/j.celrep.2021.110068)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chesnokova V, Zonis S, Barrett R, Kameda H, Wawrowsky K, Ben-Shlomo A, Yamamoto M, Gleeson J, Bresee C & Gorbunova V et al.2019 Excess growth hormone suppresses DNA damage repair in epithelial cells. JCI Insight 4 e125762. (https://doi.org/10.1172/jci.insight.125762)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chesnokova V, Zonis S, Zhou C, Recouvreux MV, Ben-Shlomo A, Araki T, Barrett R, Workman M, Wawrowsky K & Ljubimov VA et al.2016 Growth hormone is permissive for neoplastic colon growth. Proceedings of the National Academy of Sciences of the United States of America 113 E3250E3259. (https://doi.org/10.1073/pnas.1600561113)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chien CH, Lee MJ, Liou HC, Liou HH & & Fu WM 2015 Local immunosuppressive microenvironment enhances migration of melanoma cells to lungs in DJ-1 knockout mice. PLoS One 10 e0115827. (https://doi.org/10.1371/journal.pone.0115827)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chiesa J, Ferrer C, Arnould C, Vouyovitch CM, Diaz JJ, Gonzalez S, Mares P, Morel G, Wu ZS & Zhu T et al.2011 Autocrine proliferative effects of hGH are maintained in primary cultures of human mammary carcinoma cells. Journal of Clinical Endocrinology and Metabolism 96 E1418E1426. (https://doi.org/10.1210/jc.2011-0473)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chong QY, You ML, Pandey V, Banerjee A, Chen YJ, Poh HM, Zhang M, Ma L, Zhu T & Basappa S et al.2017 Release of HER2 repression of trefoil factor 3 (TFF3) expression mediates trastuzumab resistance in HER2+/ER+ mammary carcinoma. Oncotarget 8 7418874208. (https://doi.org/10.18632/oncotarget.18431)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chopin LK, Veveris-Lowe TL, Philipps AF & & Herington AC 2002 Co-expression of GH and GHR isoforms in prostate cancer cell lines. Growth Hormone and IGF Research 12 126136. (https://doi.org/10.1054/ghir.2002.0271)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Coker-Gurkan A, Celik M, Ugur M, Arisan ED, Obakan-Yerlikaya P, Durdu ZB & Palavan-Unsal N 2018 Curcumin inhibits autocrine growth hormone-mediated invasion and metastasis by targeting NF-κB signaling and polyamine metabolism in breast cancer cells. Amino Acids 50 10451069. (https://doi.org/10.1007/s00726-018-2581-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Coker-Gurkan A, Bulut D, Genc R, Arisan ED, Obakan-Yerlikaya P & & Palavan-Unsal N 2019 Curcumin prevented human autocrine growth hormone (GH) signaling mediated NF-κB activation and miR-183-96-182 cluster stimulated epithelial mesenchymal transition in T47D breast cancer cells. Molecular Biology Reports 46 355369. (https://doi.org/10.1007/s11033-018-4479-y)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Coker-Gurkan A, Ozakaltun B, Akdeniz BS, Ergen B, Obakan-Yerlikaya P, Akkoc T & & Arisan ED 2020 Proinflammatory cytokine profile is critical in autocrine GH-triggered curcumin resistance engulf by atiprimod cotreatment in MCF-7 and MDA-MB-231 breast cancer cells. Molecular Biology Reports 47 87978808. (https://doi.org/10.1007/s11033-020-05928-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cooke NE & & Liebhaber SA 1995 Molecular biology of the growth hormone-prolactin gene system. Vitamins and Hormones 50 385459. (https://doi.org/10.1016/s0083-6729(0860659-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ & & Wicha MS 2003 In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes and Development 17 12531270. (https://doi.org/10.1101/gad.1061803)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Emerald BS, Chen Y, Zhu T, Zhu Z, Lee KO, Gluckman PD & & Lobie PE 2007 AlphaCP1 mediates stabilization of hTERT mRNA by autocrine human growth hormone. Journal of Biological Chemistry 282 680690. (https://doi.org/10.1074/jbc.M600224200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Evans A, Jamieson SMF, Liu DX, Wilson WR & & Perry JK 2016 Growth hormone receptor antagonism suppresses tumour regrowth after radiotherapy in an endometrial cancer xenograft model. Cancer Letters 379 117123. (https://doi.org/10.1016/j.canlet.2016.05.031)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Frank SJ 2020 Classical and novel GH receptor signaling pathways. Molecular and Cellular Endocrinology 518 110999. (https://doi.org/10.1016/j.mce.2020.110999)

  • Frank SJ, Gilliland G, Kraft AS & & Arnold CS 1994 Interaction of the growth hormone receptor cytoplasmic domain with the JAK2 tyrosine kinase. Endocrinology 135 22282239. (https://doi.org/10.1210/endo.135.5.7956946)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gan Y, Buckels A, Liu Y, Zhang Y, Paterson AJ, Jiang J, Zinn KR & & Frank SJ 2014 Human GH receptor-IGF-1 receptor interaction: implications for GH signaling. Molecular Endocrinology (Baltimore, Md.) 28 18411854. (https://doi.org/10.1210/me.2014-1174)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gentilin E, Minoia M, Bondanelli M, Tagliati F, Degli Uberti EC & & Zatelli MC 2017 Growth hormone differentially modulates chemoresistance in human endometrial adenocarcinoma cell lines. Endocrine 56 621632. (https://doi.org/10.1007/s12020-016-1085-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Graichen R, Liu D, Sun Y, Lee KO & & Lobie PE 2002 Autocrine human growth hormone inhibits placental transforming growth factor-beta gene transcription to prevent apoptosis and allow cell cycle progression of human mammary carcinoma cells. Journal of Biological Chemistry 277 2666226672. (https://doi.org/10.1074/jbc.M109931200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gregoraszczuk EL, Milewicz T, Kolodziejczyk J, Krzysiek J, Basta A, Sztefko K, Kurek S & & Stachura J 2001 Progesterone-induced secretion of growth hormone, insulin-like growth factor I and prolactin by human breast cancer explants. Gynecological Endocrinology 15 251258. (https://doi.org/10.1080/gye.15.4.251.258)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Harvey S, Martínez-Moreno CG, Luna M & & Arámburo C 2015 Autocrine/paracrine roles of extrapituitary growth hormone and prolactin in health and disease: an overview. General and Comparative Endocrinology 220 103111. (https://doi.org/10.1016/j.ygcen.2014.11.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kahán Z, Arencibia JM, Csernus VJ, Groot K, Kineman RD, Robinson WR & & Schally AV 1999 Expression of growth hormone-releasing hormone (GHRH) messenger ribonucleic acid and the presence of biologically active GHRH in human breast, endometrial, and ovarian cancers. Journal of Clinical Endocrinology and Metabolism 84 582589. (https://doi.org/10.1210/jcem.84.2.5487)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kannan N, Kang J, Kong X, Tang J, Perry JK, Mohankumar KM, Miller LD, Liu ET, Mertani HC & Zhu T et al.2010 Trefoil factor 3 is oncogenic and mediates anti-estrogen resistance in human mammary carcinoma. Neoplasia (New York, NY) 12 10411053. (https://doi.org/10.1593/neo.10916)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kaulsay KK, Mertani HC, Lee KO & & Lobie PE 2000 Autocrine human growth hormone enhancement of human mammary carcinoma cell spreading is Jak2 dependent. Endocrinology 141 15711584. (https://doi.org/10.1210/endo.141.4.7426)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kaulsay KK, Mertani HC, Törnell J, Morel G, Lee KO & & Lobie PE 1999 Autocrine stimulation of human mammary carcinoma cell proliferation by human growth hormone. Experimental Cell Research 250 3550. (https://doi.org/10.1006/excr.1999.4492)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kaulsay KK, Zhu T, Bennett W, Lee KO & & Lobie PE 2001 The effects of autocrine human growth hormone (hGH) on human mammary carcinoma cell behavior are mediated via the hGH receptor. Endocrinology 142 767777. (https://doi.org/10.1210/endo.142.2.7936)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kong X, Wu W, Yuan Y, Pandey V, Wu Z, Lu X, Zhang W, Chen Y, Wu M & Zhang M et al.2016 Human growth hormone and human prolactin function as autocrine/paracrine promoters of progression of hepatocellular carcinoma. Oncotarget 7 2946529479. (https://doi.org/10.18632/oncotarget.8781)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kopchick JJ, Basu R, Berryman DE, Jorgensen JOL, Johannsson G & & Puri V 2022 Covert actions of growth hormone: fibrosis, cardiovascular diseases and cancer. Nature Reviews. Endocrinology 18 558573. (https://doi.org/10.1038/s41574-022-00702-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kopchick JJ, List EO, Kelder B, Gosney ES & & Berryman DE 2014 Evaluation of growth hormone (GH) action in mice: discovery of GH receptor antagonists and clinical indications. Molecular and Cellular Endocrinology 386 3445. (https://doi.org/10.1016/j.mce.2013.09.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lantinga-van Leeuwen IS, Oudshoorn M & & Mol JA 1999 Canine mammary growth hormone gene transcription initiates at the pituitary-specific start site in the absence of Pit-1. Molecular and Cellular Endocrinology 150 121128. (https://doi.org/10.1016/s0303-7207(9900010-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lantinga-van Leeuwen IS, van Garderen E, Rutteman GR & & Mol JA 2000 Cloning and cellular localization of the canine progesterone receptor: co-localization with growth hormone in the mammary gland. Journal of Steroid Biochemistry and Molecular Biology 75 219228. (https://doi.org/10.1016/s0960-0760(0000173-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lau WH, Pandey V, Kong X, Wang XN, Wu Z, Zhu T & & Lobie PE 2015 Trefoil Factor-3 (TFF3) stimulates de novo angiogenesis in mammary carcinoma both directly and indirectly via IL-8/CXCR2. PLoS One 10 e0141947. (https://doi.org/10.1371/journal.pone.0141947)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lea RW, Dawson T, Martinez-Moreno CG, El-Abry N & & Harvey S 2015 Growth hormone and cancer: GH production and action in glioma? General and Comparative Endocrinology 220 119123. (https://doi.org/10.1016/j.ygcen.2015.06.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liu N, Mertani HC, Norstedt G, Törnell J & & Lobie PE 1997 Mode of the autocrine/paracrine mechanism of growth hormone action. Experimental Cell Research 237 196206. (https://doi.org/10.1006/excr.1997.3789)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liu Y, Zhang Y, Jiang J, Lobie PE, Paulmurugan R, Langenheim JF, Chen WY, Zinn KR & & Frank SJ 2016 GHR/PRLR heteromultimer is composed of GHR homodimers and PRLR homodimers. Molecular Endocrinology (Baltimore, Md.) 30 504517. (https://doi.org/10.1210/me.2015-1319)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lombardi S, Honeth G, Ginestier C, Shinomiya I, Marlow R, Buchupalli B, Gazinska P, Brown J, Catchpole S & Liu S et al.2014 Growth hormone is secreted by normal breast epithelium upon progesterone stimulation and increases proliferation of stem/progenitor cells. Stem Cell Reports 2 780793. (https://doi.org/10.1016/j.stemcr.2014.05.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lu M, Flanagan JU, Langley RJ, Hay MP & & Perry JK 2019 Targeting growth hormone function: strategies and therapeutic applications. Signal Transduction and Targeted Therapy 4 3. (https://doi.org/10.1038/s41392-019-0036-y)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mathews LS, Enberg B & & Norstedt G 1989 Regulation of rat growth hormone receptor gene expression. Journal of Biological Chemistry 264 99059910. (https://doi.org/10.1016/S0021-9258(1881745-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mertani HC, Zhu T, Goh EL, Lee KO, Morel G & & Lobie PE 2001 Autocrine human growth hormone (hGH) regulation of human mammary carcinoma cell gene expression. Identification of CHOP as a mediator of hGH-stimulated human mammary carcinoma cell survival. Journal of Biological Chemistry 276 2146421475. (https://doi.org/10.1074/jbc.M100437200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mertani HC, Raccurt M, Abbate A, Kindblom J, Törnell J, Billestrup N, Usson Y, Morel G & & Lobie PE 2003 Nuclear translocation and retention of growth hormone. Endocrinology 144 31823195. (https://doi.org/10.1210/en.2002-221121)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Milewicz T, Gregoraszczuk EL, Augustowska K, Krzysiek J, Sztefko K & & Ryś J 2005 Progesterone but not estradiol 17beta potentiates local GH secretions by hormone-dependent breast cancer explants. An in vitro study. Experimental and Clinical Endocrinology & Diabetes 113 127132. (https://doi.org/10.1055/s-2004-830556)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Milewicz T, Ryś J, Wójtowicz A, Stochmal E, Jach R, Krzysiek J, Gregoraszczuk E, Huras H & & Dziadek O 2011 Overexpression of P53 protein and local hGH, IGF-I, IGFBP-3, IGFBP-2 and PRL secretion by human breast cancer explants. Neuro Endocrinology Letters 32 328333

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Minoia M, Gentilin E, Molè D, Rossi M, Filieri C, Tagliati F, Baroni A, Ambrosio MR, degli Uberti E & & Zatelli MC 2012 Growth hormone receptor blockade inhibits growth hormone-induced chemoresistance by restoring cytotoxic-induced apoptosis in breast cancer cells independently of estrogen receptor expression. Journal of Clinical Endocrinology and Metabolism 97 E907E916. (https://doi.org/10.1210/jc.2011-3340)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mojarrad M, Momeny M, Mansuri F, Abdolazimi Y, Tabrizi MH, Ghaffari SH, Tavangar SM & & Modarressi MH 2010 Autocrine human growth hormone expression leads to resistance of MCF-7 cells to tamoxifen. Medical Oncology (Northwood, London, England) 27 474480. (https://doi.org/10.1007/s12032-009-9237-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mol JA, Henzen-Logmans SC, Hageman P, Misdorp W, Blankenstein MA & & Rijnberk A 1995b Expression of the gene encoding growth hormone in the human mammary gland. Journal of Clinical Endocrinology and Metabolism 80 30943096. (https://doi.org/10.1210/jcem.80.10.7559904)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mol JA, Lantinga-van Leeuwen I, van Garderen E & & Rijnberk A 2000 Progestin-induced mammary growth hormone (GH) production. Advances in Experimental Medicine and Biology 480 7176. (https://doi.org/10.1007/0-306-46832-8_8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mol JA, van Garderen E, Selman PJ, Wolfswinkel J, Rijinberk A & & Rutteman GR 1995a Growth hormone mRNA in mammary gland tumors of dogs and cats. Journal of Clinical Investigation 95 20282034. (https://doi.org/10.1172/JCI117888)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Möller C, Hansson A, Enberg B, Lobie PE & & Norstedt G 1992 Growth hormone (GH) induction of tyrosine phosphorylation and activation of mitogen-activated protein kinases in cells transfected with rat GH receptor cDNA. Journal of Biological Chemistry 267 2340323408. (https://doi.org/10.1016/S0021-9258(1850105-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mukhina S, Mertani HC, Guo K, Lee KO, Gluckman PD & & Lobie PE 2004 Phenotypic conversion of human mammary carcinoma cells by autocrine human growth hormone. Proceedings of the National Academy of Sciences of the United States of America 101 1516615171. (https://doi.org/10.1073/pnas.0405881101)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Najafi M, Mortezaee K & & Majidpoor J 2019 Cancer stem cell (CSC) resistance drivers. Life Sciences 234 116781. (https://doi.org/10.1016/j.lfs.2019.116781)

  • Nakonechnaya AO, Jefferson HS, Chen X & & Shewchuk BM 2013 Differential effects of exogenous and autocrine growth hormone on LNCaP prostate cancer cell proliferation and survival. Journal of Cellular Biochemistry 114 13221335. (https://doi.org/10.1002/jcb.24473)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nakonechnaya AO & & Shewchuk BM 2015 Growth hormone enhances LNCaP prostate cancer cell motility. Endocrine Research 40 97105. (https://doi.org/10.3109/07435800.2014.966383)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nieto MA, Huang RY-J, Jackson RA & & Thiery JP 2016 EMT: 2016. Cell 166 2145. (https://doi.org/10.1016/j.cell.2016.06.028)

  • Ogawa Y, Watanabe M & & Tominaga T 2015 Prognostic factors of craniopharyngioma with special reference to autocrine/paracrine signaling: underestimated implication of growth hormone receptor. Acta Neurochirurgica 157 17311740. (https://doi.org/10.1007/s00701-015-2519-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pandey V, Perry JK, Mohankumar KM, Kong XJ, Liu SM, Wu ZS, Mitchell MD, Zhu T & & Lobie PE 2008 Autocrine human growth hormone stimulates oncogenicity of endometrial carcinoma cells. Endocrinology 149 39093919. (https://doi.org/10.1210/en.2008-0286)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pandey V, Wu ZS, Zhang M, Li R, Zhang J, Zhu T & & Lobie PE 2014 Trefoil factor 3 promotes metastatic seeding and predicts poor survival outcome of patients with mammary carcinoma. Breast Cancer Research 16 429. (https://doi.org/10.1186/s13058-014-0429-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pandey V, Zhang M, You M, Zhang W, Chen R, Zhang W, Ma L, Wu ZS, Zhu T & Xu XQ et al.2018 Expression of two non-mutated genetic elements is sufficient to stimulate oncogenic transformation of human mammary epithelial cells. Cell Death and Disease 9 1147. (https://doi.org/10.1038/s41419-018-1177-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pandey V, Zhang X, Poh HM, Wang B, Dukanya D, Ma L, Yin Z, Bender A, Periyasamy G & Zhu T et al.2022 Monomerization of homodimeric trefoil factor 3 (TFF3) by an aminonitrile compound inhibits TFF3-dependent cancer cell survival. ACS Pharmacology and Translational Science 5 761773. (https://doi.org/10.1021/acsptsci.2c00044)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Perera O, Evans A, Pertziger M, MacDonald C, Chen H, Liu DX, Lobie PE & & Perry JK 2015 Trefoil factor 3 (TFF3) enhances the oncogenic characteristics of prostate carcinoma cells and reduces sensitivity to ionising radiation. Cancer Letters 361 104111. (https://doi.org/10.1016/j.canlet.2015.02.051)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Perry JK, Wu ZS, Mertani HC, Zhu T & & Lobie PE 2017 Tumour-derived human growth hormone as a therapeutic target in oncology. Trends in Endocrinology and Metabolism 28 587596. (https://doi.org/10.1016/j.tem.2017.05.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Poh HM, Chiou YS, Chong QY, Chen RM, Rangappa KS, Ma L, Zhu T, Kumar AP, Pandey V & Basappa et al.2019 Inhibition of TFF3 enhances sensitivity-and overcomes acquired resistance-to doxorubicin in estrogen receptor-positive mammary carcinoma. Cancers 11 1528. (https://doi.org/10.3390/cancers11101528)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Propper DJ & & Balkwill FR 2022 Harnessing cytokines and chemokines for cancer therapy. Nature Reviews. Clinical Oncology 19 237253. (https://doi.org/10.1038/s41571-021-00588-9)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Raccurt M, Lobie PE, Moudilou E, Garcia-Caballero T, Frappart L, Morel G & & Mertani HC 2002 High stromal and epithelial human gh gene expression is associated with proliferative disorders of the mammary gland. Journal of Endocrinology 175 307318. (https://doi.org/10.1677/joe.0.1750307)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ranke MB & & Wit JM 2018 Growth hormone - past, present and future. Nature Reviews. Endocrinology 14 285300. (https://doi.org/10.1038/nrendo.2018.22)

  • Recouvreux MV, Wu JB, Gao AC, Zonis S, Chesnokova V, Bhowmick N, Chung LW & & Melmed S 2017 Androgen receptor regulation of local growth hormone in prostate cancer cells. Endocrinology 158 22552268. (https://doi.org/10.1210/en.2016-1939)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Robben JH, Van Garderen E, Mol JA, Wolfswinkel J & & Rijnberk A 2002 Locally produced growth hormone in canine insulinomas. Molecular and Cellular Endocrinology 197 187195. (https://doi.org/10.1016/s0303-7207(0200268-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sawada T, Arai D, Jing X, Miyajima M, Frank SJ & & Sakaguchi K 2017 Molecular interactions of EphA4, growth hormone receptor, Janus kinase 2, and signal transducer and activator of transcription 5B. PLoS One 12 e0180785. (https://doi.org/10.1371/journal.pone.0180785)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schinzel AC & & Hahn WC 2008 Oncogenic transformation and experimental models of human cancer. Frontiers in Bioscience 13 7184. (https://doi.org/10.2741/2661)

  • Schwartz DM, Bonelli M, Gadina M & & O’Shea JJ 2016 Type I/II cytokines, JAKs, and new strategies for treating autoimmune diseases. Nature Reviews. Rheumatology 12 2536. (https://doi.org/10.1038/nrrheum.2015.167)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shafiei F, Rahnama F, Pawella L, Mitchell MD, Gluckman PD & & Lobie PE 2008 DNMT3A and DNMT3B mediate autocrine hGH repression of plakoglobin gene transcription and consequent phenotypic conversion of mammary carcinoma cells. Oncogene 27 26022612. (https://doi.org/10.1038/sj.onc.1210917)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Slater M, Cooper M & & Murphy CR 2006 Human growth hormone and interleukin-6 are upregulated in endometriosis and endometrioid adenocarcinoma. Acta Histochemica 108 1318. (https://doi.org/10.1016/j.acthis.2006.01.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Slater MD & & Murphy CR 2006 Co-expression of interleukin-6 and human growth hormone in apparently normal prostate biopsies that ultimately progress to prostate cancer using low pH, high temperature antigen retrieval. Journal of Molecular Histology 37 3741. (https://doi.org/10.1007/s10735-006-9027-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stark JR, Perner S, Stampfer MJ, Sinnott JA, Finn S, Eisenstein AS, Ma J, Fiorentino M, Kurth T & Loda M et al.2009 Gleason score and lethal prostate cancer: does 3 + 4 = 4 + 3? Journal of Clinical Oncology 27 34593464. (https://doi.org/10.1200/JCO.2008.20.4669)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sustarsic EG, Junnila RK & & Kopchick JJ 2013 Human metastatic melanoma cell lines express high levels of growth hormone receptor and respond to GH treatment. Biochemical and Biophysical Research Communications 441 144150. (https://doi.org/10.1016/j.bbrc.2013.10.023)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Szepeshazi K, Schally AV, Armatis P, Groot K, Hebert F, Feil A, Varga JL & & Halmos G 2001 Antagonists of GHRH decrease production of GH and IGF-I in MXT mouse mammary cancers and inhibit tumor growth. Endocrinology 142 43714378. (https://doi.org/10.1210/endo.142.10.8426)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Takahashi Y 2017 The role of growth hormone and insulin-like growth factor-I in the liver. International Journal of Molecular Sciences 18 1447. (https://doi.org/10.3390/ijms18071447)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tang JZ, Kong XJ, Banerjee A, Muniraj N, Pandey V, Steiner M, Perry JK, Zhu T, Liu DX & & Lobie PE 2010 STAT3alpha is oncogenic for endometrial carcinoma cells and mediates the oncogenic effects of autocrine human growth hormone. Endocrinology 151 41334145. (https://doi.org/10.1210/en.2010-0273)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Timmermans-Sprang EPM, Rao NAS & & Mol JA 2008 Transactivation of a growth hormone (GH) promoter-luciferase construct in canine mammary cells. Domestic Animal Endocrinology 34 403410. (https://doi.org/10.1016/j.domaniend.2007.11.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van den Eijnden MJ & & Strous GJ 2007 Autocrine growth hormone: effects on growth hormone receptor trafficking and signaling. Molecular Endocrinology (Baltimore, Md.) 21 28322846. (https://doi.org/10.1210/me.2007-0092)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van Garderen E, de Wit M, Voorhout WF, Rutteman GR, Mol JA, Nederbragt H & & Misdorp W 1997 Expression of growth hormone in canine mammary tissue and mammary tumors. Evidence for a potential autocrine/paracrine stimulatory loop. American Journal of Pathology 150 10371047

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vouyovitch CM, Perry JK, Liu DX, Bezin L, Vilain E, Diaz JJ, Lobie PE & & Mertani HC 2016 WNT4 mediates the autocrine effects of growth hormone in mammary carcinoma cells. Endocrine-Related Cancer 23 571585. (https://doi.org/10.1530/ERC-15-0528)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang H & & Unternaehrer JJ 2019 Epithelial-mesenchymal transition and cancer stem cells: at the crossroads of differentiation and dedifferentiation. Developmental Dynamics 248 1020. (https://doi.org/10.1002/dvdy.24678)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang JJ, Chong QY, Sun XB, You ML, Pandey V, Chen YJ, Zhuang QS, Liu DX, Ma L & Wu ZS et al.2017 Autocrine hGH stimulates oncogenicity, epithelial-mesenchymal transition and cancer stem cell-like behavior in human colorectal carcinoma. Oncotarget 8 103900103918. (https://doi.org/10.18632/oncotarget.21812)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang Y, Jamieson SMF & & Perry JK 2023 Targeting growth hormone in cancer: future perspectives. Endocrine-Related Cancer 30 e230033. (https://doi.org/10.1530/ERC-23-0033)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Warren RS, Yuan H, Matli MR, Ferrara N & & Donner DB 1996 Induction of vascular endothelial growth factor by insulin-like growth factor 1 in colorectal carcinoma. Journal of Biological Chemistry 271 2948329488. (https://doi.org/10.1074/jbc.271.46.29483)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Waters MJ 2016 The growth hormone receptor. Growth Hormone and IGF Research 28 610. (https://doi.org/10.1016/j.ghir.2015.06.001)

  • Waters MJ & & Brooks AJ 2015 JAK2 activation by growth hormone and other cytokines. Biochemical Journal 466 111. (https://doi.org/10.1042/BJ20141293)

  • Watson PA, Arora VK & & Sawyers CL 2015 Emerging mechanisms of resistance to androgen receptor inhibitors in prostate cancer. Nature Reviews. Cancer 15 701711. (https://doi.org/10.1038/nrc4016)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wood TJ, Sliva D, Lobie PE, Pircher TJ, Gouilleux F, Wakao H, Gustafsson JA, Groner B, Norstedt G & & Haldosén LA 1995 Mediation of growth hormone-dependent transcriptional activation by mammary gland factor/Stat 5. Journal of Biological Chemistry 270 94489453. (https://doi.org/10.1074/jbc.270.16.9448)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu M, Zhang X, Zhang W, Yan L, Liu X, Zhang M, Pan Y, Lobie PE, Han X & & Zhu T 2023 Paracrine secretion of IL8 by breast cancer stem cells promotes therapeutic resistance and metastasis of the bulk tumor cells. Cell Communication and Signaling 21 59. (https://doi.org/10.1186/s12964-023-01068-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu ZS, Yang K, Wan Y, Qian PX, Perry JK, Chiesa J, Mertani HC, Zhu T & & Lobie PE 2011 Tumor expression of human growth hormone and human prolactin predict a worse survival outcome in patients with mammary or endometrial carcinoma. Journal of Clinical Endocrinology and Metabolism 96 E1619E1629. (https://doi.org/10.1210/jc.2011-1245)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xu J, Zhang Y, Berry PA, Jiang J, Lobie PE, Langenheim JF, Chen WY & & Frank SJ 2011 Growth hormone signaling in human T47D breast cancer cells: potential role for a growth hormone receptor-prolactin receptor complex. Molecular Endocrinology (Baltimore, Md.) 25 597610. (https://doi.org/10.1210/me.2010-0255)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xu XQ, Emerald BS, Goh ELK, Kannan N, Miller LD, Gluckman PD, Liu ET & & Lobie PE 2005 Gene expression profiling to identify oncogenic determinants of autocrine human growth hormone in human mammary carcinoma. Journal of Biological Chemistry 280 2398724003. (https://doi.org/10.1074/jbc.M503869200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yakar S, Leroith D & & Brodt P 2005 The role of the growth hormone/insulin-like growth factor axis in tumor growth and progression: lessons from animal models. Cytokine and Growth Factor Reviews 16 407420. (https://doi.org/10.1016/j.cytogfr.2005.01.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yamauchi T, Ueki K, Tobe K, Tamemoto H, Sekine N, Wada M, Honjo M, Takahashi M, Takahashi T & Hirai H et al.1997 Tyrosine phosphorylation of the EGF receptor by the kinase Jak2 is induced by growth hormone. Nature 390 9196. (https://doi.org/10.1038/36369)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yang Y, Lin Z, Lin Q, Bei W & & Guo J 2022 Pathological and therapeutic roles of bioactive peptide trefoil factor 3 in diverse diseases: recent progress and perspective. Cell Death and Disease 13 62. (https://doi.org/10.1038/s41419-022-04504-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • You ML, Chen YJ, Chong QY, Wu MM, Pandey V, Chen RM, Liu L, Ma L, Wu ZS & Zhu T et al.2017 Trefoil factor 3 mediation of oncogenicity and chemoresistance in hepatocellular carcinoma is AKT-BCL-2 dependent. Oncotarget 8 3932339344. (https://doi.org/10.18632/oncotarget.16950)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zatelli MC, Minoia M, Molè D, Cason V, Tagliati F, Margutti A, Bondanelli M, Ambrosio MR & & degli Uberti E 2009 Growth hormone excess promotes breast cancer chemoresistance. Journal of Clinical Endocrinology and Metabolism 94 39313938. (https://doi.org/10.1210/jc.2009-1026)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang W, Qian P, Zhang X, Zhang M, Wang H, Wu M, Kong X, Tan S, Ding K & Perry JK et al.2015 Autocrine/paracrine human growth hormone-stimulated microRNA 96-182-183 cluster promotes epithelial-mesenchymal transition and invasion in breast cancer. Journal of Biological Chemistry 290 1381213829. (https://doi.org/10.1074/jbc.M115.653261)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang X, Zhu T, Chen Y, Mertani HC, Lee KO & & Lobie PE 2003 Human growth hormone-regulated HOXA1 is a human mammary epithelial oncogene. Journal of Biological Chemistry 278 75807590. (https://doi.org/10.1074/jbc.M212050200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu T, Goh EL, LeRoith D & & Lobie PE 1998a Growth hormone stimulates the formation of a multiprotein signaling complex involving p130(Cas) and CrkII. Resultant activation of c-Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK). Journal of Biological Chemistry 273 3386433875. (https://doi.org/10.1074/jbc.273.50.33864)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu T, Goh EL & & Lobie PE 1998b Growth hormone stimulates the tyrosine phosphorylation and association of p125 focal adhesion kinase (FAK) with JAK2. Fak is not required for stat-mediated transcription. Journal of Biological Chemistry 273 1068210689. (https://doi.org/10.1074/jbc.273.17.10682)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu T, Ling L & & Lobie PE 2002 Identification of a JAK2-independent pathway regulating growth hormone (GH)-stimulated p44/42 mitogen-activated protein kinase activity. GH activation of Ral and phospholipase D is Src-dependent. Journal of Biological Chemistry 277 4559245603. (https://doi.org/10.1074/jbc.M201385200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu T & & Lobie PE 2000 Janus kinase 2-dependent activation of p38 mitogen-activated protein kinase by growth hormone. Resultant transcriptional activation of ATF-2 and CHOP, cytoskeletal re-organization and mitogenesis. Journal of Biological Chemistry 275 21032114. (https://doi.org/10.1074/jbc.275.3.2103)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu T, Starling-Emerald B, Zhang X, Lee KO, Gluckman PD, Mertani HC & & Lobie PE 2005a Oncogenic transformation of human mammary epithelial cells by autocrine human growth hormone. Cancer Research 65 317324. (https://doi.org/10.1158/0008-5472.317.65.1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu Z, Mukhina S, Zhu T, Mertani HC, Lee KO & & Lobie PE 2005b p44/42 MAP kinase-dependent regulation of catalase by autocrine human growth hormone protects human mammary carcinoma cells from oxidative stress-induced apoptosis. Oncogene 24 37743785. (https://doi.org/10.1038/sj.onc.1208541)

    • PubMed
    • Search Google Scholar
    • Export Citation