HSPB1 promotes tumor invasion by inducing angiogenesis in PitNETs

in Endocrine-Related Cancer
Authors:
Bin Li Department of Neurosurgery, Peking University People’s Hospital, Beijing, China

Search for other papers by Bin Li in
Current site
Google Scholar
PubMed
Close
,
Sida Zhao Department of Cell and Biology, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

Search for other papers by Sida Zhao in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-3145-705X
,
Yiyuan Chen Department of Cell and Biology, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

Search for other papers by Yiyuan Chen in
Current site
Google Scholar
PubMed
Close
,
Hua Gao Department of Cell and Biology, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

Search for other papers by Hua Gao in
Current site
Google Scholar
PubMed
Close
,
Weiyan Xie Department of Cell and Biology, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

Search for other papers by Weiyan Xie in
Current site
Google Scholar
PubMed
Close
,
Hongyun Wang Department of Cell and Biology, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China

Search for other papers by Hongyun Wang in
Current site
Google Scholar
PubMed
Close
,
Peng Zhao Department of Neurosurgical, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

Search for other papers by Peng Zhao in
Current site
Google Scholar
PubMed
Close
,
Chuzhong Li Department of Neurosurgical, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

Search for other papers by Chuzhong Li in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-0256-1261
, and
Yazhuo Zhang Department of Neurosurgical, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

Search for other papers by Yazhuo Zhang in
Current site
Google Scholar
PubMed
Close

Correspondence should be addressed to C Li or Y Zhang: lichuzhong@ccmu.edu.cn or zyz2004520@yeah.net
Restricted access
Rent on DeepDyve

Sign up for journal news

The clinical diagnosis and treatment of pituitary neuroendocrine tumors (PitNETs) that invade the cavernous sinus are fraught with difficulties and challenges. Exploring the biological characteristics involved in the occurrence and development of PitNETs that invade the cavernous sinus will help to elucidate the mechanism of cavernous sinus invasion. There are differences between intrasellar tumors (IST) and cavernous sinus-invasion tumors (CST) in ultramicrostructure, tumor microenvironment (TME), gene expression, and signaling pathways. The microvascular endothelial cell is increased in CST. The VEGFR signaling pathway, VEGF signaling pathway, and chemokine signaling pathway are activated in CST. HSPB1 is upregulated in CST and promotes cell proliferation, cell viability, and migration. HSPB1 promotes the release of VEGF from GT1-1 cells and activates the VEGF signaling pathway in bEnd.3 cells. HSPB1 promotes the migration of bEnd.3 cells to GT1-1 cells and promotes the formation of blood vessels of bEnd.3 cells. bEnd.3 cells can release CCL3 and CCL4 and promote the vitality, proliferation, and migration of GT1-1 cells. HSPB1 promotes the formation of blood vessels of bEnd.3 cells and ultimately leads to tumor growth in vivo. HSPB1 acts as a key gene for invasion of the cavernous sinus in PitNETs, remodeling TME by promoting the formation of blood vessels of brain microvascular endothelial cells. The synergistic effect of tumor cells and microvascular endothelial cells promotes tumor progression. The mechanism by which HSPB1 promotes tumor invasion by inducing angiogenesis in PitNETs may be a new target for the treatment of PitNETs invading the cavernous sinus.

 

  • Collapse
  • Expand
  • Acunzo J, Katsogiannou M & & Rocchi P 2012 Small heat shock proteins HSP27 (HspB1), alphaB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death. International Journal of Biochemistry and Cell Biology 44 16221631. (https://doi.org/10.1016/j.biocel.2012.04.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aran D, Hu Z & & Butte AJ 2017 xCell: digitally portraying the tissue cellular heterogeneity landscape. Genome Biology 18 220. (https://doi.org/10.1186/s13059-017-1349-1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Assi T, Watson S, Samra B, Rassy E, Le Cesne A, Italiano A & & Mir O 2021 Targeting the VEGF pathway in osteosarcoma. Cells 10. (https://doi.org/10.3390/cells10051240)

  • Cheslow L & & Alvarez JI 2016 Glial-endothelial crosstalk regulates blood-brain barrier function. Current Opinion in Pharmacology 26 3946. (https://doi.org/10.1016/j.coph.2015.09.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Concannon CG, Gorman AM & & Samali A 2003 On the role of Hsp27 in regulating apoptosis. Apoptosis 8 6170. (https://doi.org/10.1023/a:1021601103096)

  • Han C, Lin S, Lu X, Xue L & & Wu ZB 2021 Tumor-associated macrophages: new horizons for pituitary adenoma researches. Frontiers in Endocrinology 12 785050. (https://doi.org/10.3389/fendo.2021.785050)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hanahan D & & Weinberg RA 2011 Hallmarks of cancer: the next generation. Cell 144 646674. (https://doi.org/10.1016/j.cell.2011.02.013)

  • Hlavac M, Knoll A, Etzrodt-Walter G, Sommer F, Scheithauer M, Coburger J, Wirtz CR & & Pala A 2019 Intraoperative MRI in transsphenoidal resection of invasive pituitary macroadenomas. Neurosurgical Review 42 737743. (https://doi.org/10.1007/s10143-019-01102-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ilie MD, Vasiljevic A, Bertolino P & & Raverot G 2023 Biological and therapeutic implications of the tumor microenvironment in pituitary adenomas. Endocrine Reviews 44 297311. (https://doi.org/10.1210/endrev/bnac024)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kauppinen-Makelin R, Sane T, Sintonen H, Markkanen H, Valimaki MJ, Loyttyniemi E, Niskanen L, Reunanen A & & Stenman UH 2006 Quality of life in treated patients with acromegaly. Journal of Clinical Endocrinology and Metabolism 91 38913896. (https://doi.org/10.1210/jc.2006-0676)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Korbecki J, Kojder K, Siminska D, Bohatyrewicz R, Gutowska I, Chlubek D & & Baranowska-Bosiacka I 2020 CC chemokines in a tumor: a review of pro-cancer and anti-cancer properties of the ligands of receptors CCR1, CCR2, CCR3, and CCR4. International Journal of Molecular Sciences 21. (https://doi.org/10.3390/ijms21218412)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lake MG, Krook LS & & Cruz SV 2013 Pituitary adenomas: an overview. American Family Physician 88 319327.

  • Lee YJ, Lee HJ, Choi SH, Jin YB, An HJ, Kang JH, Yoon SS & & Lee YS 2012 Soluble HSPB1 regulates VEGF-mediated angiogenesis through their direct interaction. Angiogenesis 15 229242. (https://doi.org/10.1007/s10456-012-9255-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li B, Cheng J, Wang H, Zhao S, Zhu H, Li C, Zhang Y & & Zhao P 2019 CCNB1 affects cavernous sinus invasion in pituitary adenomas through the epithelial-mesenchymal transition. Journal of Translational Medicine 17 336. (https://doi.org/10.1186/s12967-019-2088-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li BH, Garstka MA & & Li ZF 2020 Chemokines and their receptors promoting the recruitment of myeloid-derived suppressor cells into the tumor. Molecular Immunology 117 201215. (https://doi.org/10.1016/j.molimm.2019.11.014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liotti F, Marotta M, Melillo RM & & Prevete N 2022 The impact of resolution of inflammation on tumor microenvironment: exploring new ways to control cancer progression. Cancers 14. (https://doi.org/10.3390/cancers14143333)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marques P, Barry S, Carlsen E, Collier D, Ronaldson A, Awad S, Dorward N, Grieve J, Mendoza N, Muquit S, et al.2019 Chemokines modulate the tumour microenvironment in pituitary neuroendocrine tumours. Acta Neuropathologica Communications 7 172. (https://doi.org/10.1186/s40478-019-0830-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marques P, Barry S, Carlsen E, Collier D, Ronaldson A, Dorward N, Grieve J, Mendoza N, Nair R, Muquit S, et al.2020 The role of the tumour microenvironment in the angiogenesis of pituitary tumours. Endocrine 70 593606. (https://doi.org/10.1007/s12020-020-02478-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marques P & & Korbonits M 2023 Tumour microenvironment and pituitary tumour behaviour. Journal of Endocrinological Investigation 46 10471063. (https://doi.org/10.1007/s40618-023-02089-1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marques P, Silva AL, Lopez-Presa D, Faria C & & Bugalho MJ 2022 The microenvironment of pituitary adenomas: biological, clinical and therapeutical implications. Pituitary 25 363382. (https://doi.org/10.1007/s11102-022-01211-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Melmed S, Kaiser UB, Lopes MB, Bertherat J, Syro LV, Raverot G, Reincke M, Johannsson G, Beckers A, Fleseriu M, et al.2022 Clinical biology of the pituitary adenoma. Endocrine Reviews 43 10031037. (https://doi.org/10.1210/endrev/bnac010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Micko A, Oberndorfer J, Weninger WJ, Vila G, Hoftberger R, Wolfsberger S & & Knosp E 2019 Challenging Knosp high-grade pituitary adenomas. Journal of Neurosurgery 132 17391746. (https://doi.org/10.3171/2019.3.JNS19367)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mirandola L, Figueroa JA, Phan TT, Grizzi F, Kim M, Rahman RL, Jenkins MR, Cobos E, Jumper C, Alalawi R, et al.2015 Novel antigens in non-small cell lung cancer: SP17, AKAP4, and PTTG1 are potential immunotherapeutic targets. Oncotarget 6 28122826. (https://doi.org/10.18632/oncotarget.2802)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mukaida N, Sasaki SI & & Baba T 2020 CCL4 signaling in the tumor microenvironment. Advances in Experimental Medicine and Biology 1231 2332. (https://doi.org/10.1007/978-3-030-36667-4_3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Niu J, Zhang S, Ma S, Diao J, Zhou W, Tian J, Zang Y & & Jia W 2019 Preoperative prediction of cavernous sinus invasion by pituitary adenomas using a radiomics method based on magnetic resonance images. European Radiology 29 16251634. (https://doi.org/10.1007/s00330-018-5725-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ntanasis-Stathopoulos I, Fotiou D & & Terpos E 2020 CCL3 signaling in the tumor microenvironment. Advances in Experimental Medicine and Biology 1231 1321. (https://doi.org/10.1007/978-3-030-36667-4_2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Qin W, Zhang J, Rong R, Zhang L, Gao H, Liu C, Ren Q, Zheng G, Wang J, Meng L, et al.2022 Osteoglycin (OGN) promotes tumorigenesis of pancreatic cancer cell via targeting ID4. Tissue and Cell 78 101867. (https://doi.org/10.1016/j.tice.2022.101867)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sato M, Tamura R, Tamura H, Mase T, Kosugi K, Morimoto Y, Yoshida K & & Toda M 2019 Analysis of tumor angiogenesis and immune microenvironment in non-functional pituitary endocrine tumors. Journal of Clinical Medicine 8. (https://doi.org/10.3390/jcm8050695)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Serioli S, Doglietto F, Fiorindi A, Biroli A, Mattavelli D, Buffoli B, Ferrari M, Cornali C, Rodella L, Maroldi R, et al.2019 Pituitary adenomas and invasiveness from anatomo-surgical, radiological, and histological perspectives: a systematic literature review. Cancers 11. (https://doi.org/10.3390/cancers11121936)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sonal S, Deshpande V, Ting DT, Cusack JC, Parikh AR, Neyaz A, Pankaj A, Taylor MS, Dinaux AM, Leijssen LGJ, et al.2022 Molecular basis of extramural vascular invasion (EMVI) in colorectal carcinoma. Annals of Surgical Oncology 29 73727382. (https://doi.org/10.1245/s10434-022-12212-w)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tanimura S, Hirano AI, Hashizume J, Yasunaga M, Kawabata T, Ozaki K & & Kohno M 2007 Anticancer drugs up-regulate HspBP1 and thereby antagonize the prosurvival function of Hsp70 in tumor cells. Journal of Biological Chemistry 282 3543035439. (https://doi.org/10.1074/jbc.M707547200)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Testa E, Palazzo C, Mastrantonio R & & Viscomi MT 2022 Dynamic interactions between tumor cells and brain microvascular endothelial cells in glioblastoma. Cancers 14. (https://doi.org/10.3390/cancers14133128)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tomlinson JW, Holden N, Hills RK, Wheatley K, Clayton RN, Bates AS, Sheppard MC, Stewart PM & & Hypopituita WMP 2001 Association between premature mortality and hypopituitarism. West Midlands Prospective Hypopituitary Study Group. Lancet 357 425431. (https://doi.org/10.1016/s0140-6736(0004006-x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wettstein G, Bellaye PS, Micheau O & & Bonniaud P 2012 Small heat shock proteins and the cytoskeleton: an essential interplay for cell integrity? International Journal of Biochemistry and Cell Biology 44 16801686. (https://doi.org/10.1016/j.biocel.2012.05.024)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Winkler EA, Bell RD & & Zlokovic BV 2011 Central nervous system pericytes in health and disease. Nature Neuroscience 14 13981405. (https://doi.org/10.1038/nn.2946)

  • Wu J, Liu T, Rios Z, Mei Q, Lin X & & Cao S 2017 Heat shock proteins and cancer. Trends in Pharmacological Sciences 38 226256. (https://doi.org/10.1016/j.tips.2016.11.009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang A, Xu Y, Xu H, Ren J, Meng T, Ni Y, Zhu Q, Zhang WB, Pan YB, Jin J, et al.2021 Lactate-induced M2 polarization of tumor-associated macrophages promotes the invasion of pituitary adenoma by secreting CCL17. Theranostics 11 38393852. (https://doi.org/10.7150/thno.53749)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zheng S, Liu B & & Guan X 2022 The role of tumor microenvironment in invasion and metastasis of esophageal squamous cell carcinoma. Frontiers in Oncology 12 911285. (https://doi.org/10.3389/fonc.2022.911285)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhou S, Lan Y, Li Y, Li Z, Pu J & & Wei L 2022 Hypoxic tumor-derived exosomes induce M2 macrophage polarization via PKM2/AMPK to promote lung cancer progression. Cell Transplantation 31 9636897221106998. (https://doi.org/10.1177/09636897221106998)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu H, Guo J, Shen Y, Dong W, Gao H, Miao Y, Li C & & Zhang Y 2018 Functions and mechanisms of tumor necrosis factor-alpha and noncoding RNAs in bone-invasive pituitary adenomas. Clinical Cancer Research 24 57575766. (https://doi.org/10.1158/1078-0432.CCR-18-0472)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu HB, Li B, Guo J, Miao YZ, Shen YT, Zhang YZ, Zhao P & & Li CZ 2021 LncRNA MEG8 promotes TNF-alpha expression by sponging miR-454-3p in bone-invasive pituitary adenomas. Aging 13 1434214354. (https://doi.org/10.18632/aging.203048)

    • PubMed
    • Search Google Scholar
    • Export Citation