Functional consequences of prolactin signalling in endothelial cells: A potential link with angiogenesis in pathophysiology?

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 9, 2012, Pages 2035-2048

  Reuwer, Anne Q ^a,b   Nowak Sliwinska, Patrycja ^c   Mans, Laurie A ^c   van der Loos, Chris M ^a   von der Thüsen, Jan H ^d   Twickler, Marcel Th B ^a,e   Spek, C Arnold ^a   Goffin, Vincent ^f   Griffioen, Arjan W ^c   Borensztajn, Keren S ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b Tergooiziekenhuizen ^*  (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MEDICAL CENTER HAAGLANDEN   (Netherlands)

^e ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^f INSERM   (France)

Author keywords

Angiogenesis; Endothelial cells; Pathophysiology; Prolactin; Prolactin receptor

Indexed keywords

ANGIOGENIC FACTOR; COLLAGEN; LAMININ; MATRIGEL; PROLACTIN; PROLACTIN RECEPTOR; PROLACTIN, ARG(129); PROLACTIN, ARG(129)-; PROTEOGLYCAN; STAT5 PROTEIN;

ANIMAL; ARTICLE; BREAST TUMOR; CELL LINE; CHICK EMBRYO; DRUG ANTAGONISM; DRUG COMBINATION; DRUG EFFECT; ENDOTHELIUM CELL; FEMALE; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; BREAST NEOPLASMS; CELL LINE; CHICK EMBRYO; COLLAGEN; DRUG COMBINATIONS; ENDOTHELIAL CELLS; FEMALE; IMMUNOHISTOCHEMISTRY; LAMININ; MAP KINASE SIGNALING SYSTEM; MICE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROLACTIN; PROTEOGLYCANS; RECEPTORS, PROLACTIN; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR;

EID: 84865444754     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01499.x     Document Type: Article

References (84)

1. Horseman ND. Prolactin and mammary gland development. J Mammary Gland Biol Neoplasia. 1999; 4: 79-88.
2. Bole-Feysot C, Goffin V, Edery M, et al Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev. 1998; 19: 225-68.
3. Ben-Jonathan N, LaPensee CR, LaPensee EW. What can we learn from rodents about prolactin in humans?Endocr Rev. 2008; 29: 1-41.
4. Nagano M, Chastre E, Choquet A, et al Expression of prolactin and growth hormone receptor genes and their isoforms in the gastrointestinal tract. Am J Physiol. 1995; 268: G431-42.
5. Peirce SK, Chen WY, Chen WY. Quantification of prolactin receptor mRNA in multiple human tissues and cancer cell lines by real time RT-PCR. J Endocrinol. 2001; 171: R1-4.
6. Gout PW, Beer CT, Noble RL. Prolactin-stimulated growth of cell cultures established from malignant Nb rat lymphomas. Cancer Res. 1980; 40: 2433-6.
7. Tworoger SS, Hankinson SE. Prolactin and breast cancer etiology: an epidemiologic perspective. J Mammary Gland Biol Neoplasia. 2008; 13: 41-53.
8. Bogorad RL, Courtillot C, Mestayer C, et al Identification of a gain-of-function mutation of the prolactin receptor in women with benign breast tumours. Proc Natl Acad Sci USA. 2008; 105: 14533-8.
9. Goffin V, Bogorad RL, Touraine P. Identification of gain-of-function variants of the human prolactin receptor. Methods Enzymol. 2010; 484: 329-55.
10. Nyante SJ, Faupel-Badger JM, Sherman ME, et al Genetic variation in PRL and PRLR, and relationships with serum prolactin levels and breast cancer risk: results from a population-based case-control study in Poland. Breast Cancer Res. 2011; 13: R42.
11. Fernandez I, Touraine P, Goffin V. Prolactin and human tumourogenesis. J Neuroendocrinol. 2010; 22: 771-7.
12. Clevenger CV, Furth PA, Hankinson SE, et al The role of prolactin in mammary carcinoma. Endocr Rev. 2003; 24: 1-27.
13. Corbacho AM, Valacchi G, Kubala L, et al Tissue-specific gene expression of prolactin receptor in the acute-phase response induced by lipopolysaccharides. Am J Physiol Endocrinol Metab. 2004; 287: E750-7.
14. Nagano M, Kelly PA. Tissue distribution and regulation of rat prolactin receptor gene expression. Quantitative analysis by polymerase chain reaction. J Biol Chem. 1994; 269: 13337-45.
15. Bernichtein S, Touraine P, Goffin V. New concepts in prolactin biology. J Endocrinol. 2010; 206: 1-11.
16. Erdmann S, Ricken A, Merkwitz C, et al The expression of prolactin and its cathepsin D-mediated cleavage in the bovine corpus luteum vary with the estrous cycle. Am J Physiol Endocrinol Metab. 2007; 293: E1365-77.
17. Grosdemouge I, Bachelot A, Lucas A, et al Effects of deletion of the prolactin receptor on ovarian gene expression. Reprod Biol Endocrinol. 2003; 1: 12.
18. Ko JY, Ahn YL, Cho BN. Angiogenesis and white blood cell proliferation induced in mice by injection of a prolactin-expressing plasmid into muscle. Mol Cells. 2003; 15: 262-70.
19. Struman I, Bentzien F, Lee H, et al Opposing actions of intact and N-terminal fragments of the human prolactin/growth hormone family members on angiogenesis: an efficient mechanism for the regulation of angiogenesis. Proc Natl Acad Sci USA. 1999; 96: 1246-51.
20. Goldhar AS, Vonderhaar BK, Trott JF, et al Prolactin-induced expression of vascular endothelial growth factor via Egr-1. Mol Cell Endocrinol. 2005; 232: 9-19.
21. Malaguarnera L, Imbesi R, Di RM, et al Action of prolactin, IFN-gamma, TNF-alpha and LPS on heme oxygenase-1 expression and VEGF release in human monocytes/macrophages. Int Immunopharmacol. 2005; 5: 1458-69.
22. Merkle CJ, Schuler LA, Schaeffer RC Jr, et al Structural and functional effects of high prolactin levels on injured endothelial cells: evidence for an endothelial prolactin receptor. Endocrine. 2000; 13: 37-46.
23. Ricken AM, Traenkner A, Merkwitz C, et al The short prolactin receptor predominates in endothelial cells of micro- and macrovascular origin. J Vasc Res. 2007; 44: 19-30.
24. Clapp C, Thebault S, de la Escalera Martínez G. Role of prolactin and vasoinhibins in the regulation of vascular function in mammary gland. J Mammary Gland Biol Neoplasia. 2008; 13: 55-67.
25. Borensztajn K, Aberson H, Peppelenbosch MP, et al FXa-induced intracellular signaling links coagulation to neoangiogenesis: potential implications for fibrosis. Biochim Biophys Acta. 2009; 1793: 798-805.
26. Walter-Yohrling J, Morgenbesser S, Rouleau C, et al Murine endothelial cell lines as models of tumour endothelial cells. Clin Cancer Res. 2004; 10: 2179-89.
27. van Beijnum JR, Dings RP, van der Linden E, et al Gene expression of tumour angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood. 2006; 108: 2339-48.
28. Bernichtein S, Kayser C, Dillner K, et al Development of pure prolactin receptor antagonists. J Biol Chem. 2003; 278: 35988-99.
29. Rouet V, Bogorad RL, Kayser C, et al Local prolactin is a target to prevent expansion of basal/stem cells in prostate tumours. Proc Natl Acad Sci USA. 2010; 107: 15199-204.
30. Nowak-Sliwinska P, van Beijnum JR, van Berkel M, et al Vascular regrowth following photodynamic therapy in the chicken embryo chorioallantoic membrane. Angiogenesis. 2010; 13: 281-92.
31. Nowak-Sliwinska P, Ballini JP, Wagnieres G, et al Processing of fluorescence angiograms for the quantification of vascular effects induced by anti-angiogenic agents in the CAM model. Microvasc Res. 2010; 79: 21-8.
32. Borensztajn K, Stiekema J, Nijmeijer S, et al Factor Xa stimulates proinflammatory and profibrotic responses in fibroblasts via protease-activated receptor-2 activation. Am J Pathol. 2008; 172: 309-20.
33. Nowak-Sliwinska P, van Beijnum JR, Casini A, et al Organometallic ruthenium(II) arene compounds with antiangiogenic activity. J Med Chem. 2011; 54: 3895-902.
34. Brandwijk RJ, Nesmelova I, Dings RP, et al Cloning an artificial gene encoding angiostatic anginex: from designed peptide to functional recombinant protein. Biochem Biophys Res Commun. 2005; 333: 1261-8.
35. Bijlsma MF, Borensztajn KS, Roelink H, et al Sonic hedgehog induces transcription-independent cytoskeletal rearrangement and migration regulated by arachidonate metabolites. Cell Signal. 2007; 19: 2596-604.
36. Michail S, Abernathy F. A new model for studying eosinophil migration across cultured intestinal epithelial monolayers. J Pediatr Gastroenterol Nutr. 2004; 39: 56-63.
37. van der Schaft DW, Dings RP, de Lussanet QG, et al The designer anti-angiogenic peptide anginex targets tumour endothelial cells and inhibits tumour growth in animal models. FASEB J. 2002; 16: 1991-3.
38. Aranda E, Owen GI. A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA.hy926 endothelial cell line. Biol Res. 2009; 42: 377-89.
39. Friedli A, Fischer E, Novak-Hofer I, et al The soluble form of the cancer-associated Ll cell adhesion molecule is a pro-angiogenic factor. Int J Biochem Cell Biol. 2009; 41: 1572-80.
40. Xu H, Czerwinski P, Hortmann M, et al Protein kinase C alpha promotes angiogenic activity of human endothelial cells via induction of vascular endothelial growth factor. Cardiovasc Res. 2008; 78: 349-55.
41. Sakai T, Balasubramanian K, Maiti S, et al Plasmin-cleaved beta-2-glycoprotein 1 is an inhibitor of angiogenesis. Am J Pathol 2007; 171: 1659-69.
42. Piqueras L, Reynolds AR, Hodivala-Dilke KM, et al Activation of PPARbeta/delta induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol. 2007; 27: 63-9.
43. Streefkerk JG, de Graaf GA, de Vries RA. Antibody against horse radish peroxidase in lymphoid organs. Acta Morphol Neerl Scand. 1972; 10: 398-9.
44. Galsgaard ED, Rasmussen BB, Folkesson CG, et al Re-evaluation of the prolactin receptor expression in human breast cancer. J Endocrinol. 2009; 201: 115-28.
45. van der Loos CM. Multiple immunoenzyme staining: methods and visualizations for the observation with spectral imaging. J Histochem Cytochem. 2008; 56: 313-28.
46. Makanya AN, Hlushchuk R, Djonov VG. Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling. Angiogenesis. 2009; 12: 113-23.
47. Saaristo A, Veikkola T, Enholm B, et al Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J. 2002; 16: 1041-9.
48. Reuwer AQ, van Eijk M, Houttuijn-Bloemendaal FM, et al The prolactin receptor is expressed in macrophages within human carotid atherosclerotic plaques: a role for prolactin in atherogenesis?J Endocrinol. 2011; 208: 107-17.
49. van der Loos CM, Teeling P. A generally applicable sequential alkaline phosphatase immunohistochemical double staining. J Histotechnol. 2008; 31: 119-27.
50. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005; 438: 932-6.
51. Shiojima I, Sato K, Izumiya Y, et al Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005; 115: 2108-18.
52. Molin D, Post MJ. Therapeutic angiogenesis in the heart: protect and serve. Curr Opin Pharmacol. 2007; 7: 158-63.
53. Levine RJ, Maynard SE, Qian C, et al Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004; 350: 672-83.
54. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell. 1991; 64: 327-36.
55. Kuiper EJ, Van Nieuwenhoven FA, de Smet MD, et al The angio-fibrotic switch of VEGF and CTGF in proliferative diabetic retinopathy. PLoS One. 2008; 3: e2675.
56. Marrelli A, Cipriani P, Liakouli V, et al Angiogenesis in rheumatoid arthritis: a disease specific process or a common response to chronic inflammation?Autoimmun Rev. 2011; 10: 595-8.
57. Yang X, Qiao D, Meyer K, et al Signal transducers and activators of transcription mediate fibroblast growth factor-induced vascular endothelial morphogenesis. Cancer Res. 2009; 69: 1668-77.
58. Rafiee P, Heidemann J, Ogawa H, et al Cyclosporin A differentially inhibits multiple steps in VEGF induced angiogenesis in human microvascular endothelial cells through altered intracellular signaling. Cell Commun Signal. 2004; 2: 3.
59. Wang XH, Xu B, Liu JT, et al Effect of beta-escin sodium on endothelial cells proliferation, migration and apoptosis. Vascul Pharmacol. 2008; 49: 158-65.
60. Binion DG, Otterson MF, Rafiee P. Curcumin inhibits VEGF-mediated angiogenesis in human intestinal microvascular endothelial cells through COX-2 and MAPK inhibition. Gut. 2008; 57: 1509-17.
61. Mofarrahi M, Hussain SN. Expression and functional roles of angiopoietin-2 in skeletal muscles. PLoS One. 2011; 6: e22882.
62. Perera PM, Wypasek E, Madhavan S, et al Mechanical signals control SOX-9, VEGF, and c-Myc expression and cell proliferation during inflammation via integrin-linked kinase, B-Raf, and ERK1/2-dependent signaling in articular chondrocytes. Arthritis Res Ther. 2010; 12: R106.
63. Farooq F, Molina FA, Hadwen J, et al Prolactin increases SMN expression and survival in a mouse model of severe spinal muscular atrophy via the STAT5 pathway. J Clin Invest. 2011; 121: 3042-50.
64. Cheranov SY, Wang D, Kundumani-Sridharan V, et al The 15(S)-hydroxyeicosatetraenoic acid-induced angiogenesis requires Janus kinase 2-signal transducer and activator of transcription-5B-dependent expression of interleukin-8. Blood. 2009; 113: 6023-33.
65. Goffin V, Kinet S, Ferrag F, et al Antagonistic properties of human prolactin analogs that show paradoxical agonistic activity in the Nb2 bioassay. J Biol Chem. 1996; 271: 16573-9.
66. Kinet S, Bernichtein S, Kelly PA, et al Biological properties of human prolactin analogs depend not only on global hormone affinity, but also on the relative affinities of both receptor binding sites. J Biol Chem. 1999; 274: 26033-43.
67. Kurtz A, Bristol LA, Toth BE, et al Mammary epithelial cells of lactating rats express prolactin messenger ribonucleic acid. Biol Reprod. 1993; 48: 1095-103.
68. Mershon J, Sall W, Mitchner N, et al Prolactin is a local growth factor in rat mammary tumours. Endocrinology. 1995; 136: 3619-23.
69. Doll F, Pfeilschifter J, Huwiler A. Prolactin upregulates sphingosine kinase-1 expression and activity in the human breast cancer cell line MCF7 and triggers enhanced proliferation and migration. Endocr Relat Cancer. 2007; 14: 325-35.
70. Maus MV, Reilly SC, Clevenger CV. Prolactin as a chemoattractant for human breast carcinoma. Endocrinology. 1999; 140: 5447-50.
71. Miller SL, Antico G, Raghunath PN, et al Nek3 kinase regulates prolactin-mediated cytoskeletal reorganization and motility of breast cancer cells. Oncogene. 2007; 26: 4668-78.
72. Howell SJ, Anderson E, Hunter T, et al Prolactin receptor antagonism reduces the clonogenic capacity of breast cancer cells and potentiates doxorubicin and paclitaxel cytotoxicity. Breast Cancer Res. 2008; 10: R68.
73. Patan S. Vasculogenesis and angiogenesis. Cancer Treat Res. 2004; 117: 3-32.
74. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology. 2005; 69(Suppl 3): 4-10.
75. Clapp C, Martial JA, Guzman RC, et al The 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinology. 1993; 133: 1292-9.
76. Ferrara N, Clapp C, Weiner R. The 16K fragment of prolactin specifically inhibits basal or fibroblast growth factor stimulated growth of capillary endothelial cells. Endocrinology. 1991; 129: 896-900.
77. Ochoa A, Montes de Oca P, Rivera JC, et al Expression of prolactin gene and secretion of prolactin by rat retinal capillary endothelial cells. Invest Ophthalmol Vis Sci. 2001; 42: 1639-45.
78. Castilla A, Garcia C, Cruz-Soto M, et al Prolactin in ovarian follicular fluid stimulates endothelial cell proliferation. J Vasc Res. 2010; 47: 45-53.
79. Malaguarnera L, Pilastro MR, Quan S, et al Significance of heme oxygenase in prolactin-mediated cell proliferation and angiogenesis in human endothelial cells. Int J Mol Med. 2002; 10: 433-40.
80. McHale K, Tomaszewski JE, Puthiyaveettil R, et al Altered expression of prolactin receptor-associated signaling proteins in human breast carcinoma. Mod Pathol. 2008; 21: 565-71.
81. Clapp C, Thebault S, Jeziorski MC, et al Peptide hormone regulation of angiogenesis. Physiol Rev. 2009; 89: 1177-215.
82. Huang K, Ueda E, Chen Y, et al Paradigm-shifters: phosphorylated prolactin and short prolactin receptors. J Mammary Gland Biol Neoplasia. 2008; 13: 69-79.
83. Clapp C, Weiner RI. A specific, high affinity, saturable binding site for the 16-kilodalton fragment of prolactin on capillary endothelial cells. Endocrinology. 1992; 130: 1380-6.
84. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995; 1: 27-31.