The multifaceted actions of PTHrP in skeletal metastasis

Future Oncology

Volumn 8, Issue 7, 2012, Pages 803-817

  Soki, Fabiana N ^a   Park, Serk In ^a   McCauley, Laurie K ^a,b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

bone; breast cancer; metastasis; parathyroid hormone related protein; premetastatic niche; prostate cancer; PTHrP

Indexed keywords

4 (3 BROMOANILINO) 6,7 DIMETHOXYQUINAZOLINE; ERLOTINIB; GEFITINIB; GROWTH FACTOR; PARATHYROID HORMONE; PTHRP HORMONE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANOIKIS; APOPTOSIS; AUTOCRINE EFFECT; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; INTRACRINE SIGNALLING; MUSCLE METASTASIS; NONHUMAN; ONCOLOGICAL PARAMETERS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE METASTSIS; TUMOR DORMANCY; TUMOR MICROENVIRONMENT;

ANOIKIS; APOPTOSIS; BONE AND BONES; BONE NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; CELLULAR MICROENVIRONMENT; HUMANS; HYPERCALCEMIA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PARATHYROID HORMONE-RELATED PROTEIN; TUMOR MICROENVIRONMENT;

EID: 84864453110     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.12.76     Document Type: Review

References (102)

1. Mundy GR. Metastasis to bone: Causes, consequences and therapeutic opportunities. Nat. Rev. Cancer 2(8), 584-593 (2002).
2. McCauley LK, Martin TJ. Twenty-five years of PTHrP progress from cancer hormone to multi-functional cytokine. J. Bone Miner. Res. 27(6), 1231-1239 (2012).
3. Kramer B, Tisdall FF. A simple technique for the determination of calcium and magnesium in small amounts of serum. J. Biol. Chem. 47(3), 475-481 (1921).
4. Albright F. Case records of the Massachusetts General Hospital. N. Engl. J. Med. 225, 789-791, Case 27461 (1941).
5. Clines GA, Guise TA. Hypercalcaemia of malignancy and basic research on mechanisms responsible for osteolytic and osteoblastic metastasis to bone. Endocr. Relat. Cancer 12(3), 549-583 (2005).
6. Manring MM, Calhoun JH. Biographical sketch: FULLER Albright, MD 1900-1969. Clin. Orthop. Relat. Res. 469(8), 2092-2095 (2011).
7. Suva LJ, Winslow GA, Wettenhall RE et al. A parathyroid hormone-related protein implicated in malignant hypercalcemia: Cloning and expression. Science 237(4817), 893-896 (1987).
8. Strewler GJ, Stern PH, Jacobs JW et al. Parathyroid hormone-like protein from human renal carcinoma cells. Structural and functional homology with parathyroid hormone. J. Clin. Invest. 80(6), 1803-1807 (1987).
9. Burtis WJ, Wu T, Bunch C et al. Identification of a novel 17,000-dalton parathyroid hormone-like adenylate cyclase-stimulating protein from a tumor associated with humoral hypercalcemia of malignancy. J. Biol. Chem. 262(15), 7151-7156 (1987).
10. Stewart AF, Burtis WJ, Wu T, Goumas D, Broadus AE. Two forms of parathyroid hormone-like adenylate cyclase-stimulating protein derived from tumors associated with humoral hypercalcemia of malignancy. J. Bone Miner. Res. 2(6), 587-593 (1987).
11. Schilling T, Pecherstorfer M, Blind E, Leidig G, Ziegler R, Raue F. Parathyroid hormone-related protein (PTHrP) does not regulate 1,25-dihydroxyvitamin D serum levels in hypercalcemia of malignancy. J. Clin. Endocrinol. Metab. 76(3), 801-803 (1993).
12. Nakayama K, Fukumoto S, Takeda S et al. Differences in bone and vitamin D metabolism between primary hyperparathyroidism and malignancy-associated hypercalcemia. J. Clin. Endocrinol. Metab. 81(2), 607-611 (1996).
13. Seymour JF, Gagel RF. Calcitriol: The major humoral mediator of hypercalcemia in Hodgkin's disease and non-Hodgkin's lymphomas. Blood 82(5), 1383-1394 (1993).
14. Martin TJ, Moseley JM, Gillespie MT. Parathyroid hormone-related protein: Biochemistry and molecular biology. Crit. Rev. Biochem. Mol. Biol. 26(3-4), 377-395 (1991).
15. De Castro LF, Lozano D, Portal-Nunez S et al. Comparison of the skeletal effects induced by daily administration of PTHrP (1-36) and PTHrP (107-139) to ovariectomized mice. J. Cell. Physiol. 227(4), 1752-1760 (2012).
16. Karaplis AC, Luz A, Glowacki J et al. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8(3), 277-289 (1994).
17. Amizuka N, Warshawsky H, Henderson JE, Goltzman D, Karaplis AC. Parathyroid hormone-related peptide-depleted mice show abnormal epiphyseal cartilage development and altered endochondral bone formation. J. Cell Biol. 126(6), 1611-1623 (1994).
18. Amizuka N, Goltzman D, Ozawa H. The biologic action of parathyroid hormone-related peptide on bone and cartilage cells. Tissue Eng. 2(4), 277-287 (1996).
19. Kong XF, Schipani E, Lanske B et al. The rat, mouse and human genes encoding the receptor for parathyroid hormone and parathyroid hormone-related peptide are highly homologous. Biochem. Biophys. Res. Commun. 200(3), 1290-1299 (1994).
20. Downey SE, Hoyland J, Freemont AJ, Knox F, Walls J, Bundred NJ. Expression of the receptor for parathyroid hormone-related protein in normal and malignant breast tissue. J. Pathol. 183(2), 212-217 (1997).
21. Asadi F, Farraj M, Sharifi R, Malakouti S, Antar S, Kukreja S. Enhanced expression of parathyroid hormone-related protein in prostate cancer as compared with benign prostatic hyperplasia. Hum. Pathol. 27(12), 1319-1323 (1996).
22. Fuller K, Owens JM, Chambers TJ. Induction of osteoclast formation by parathyroid hormone depends on an action on stromal cells. J. Endocrinol. 158(3), 341-350 (1998).
23. Datta NS, Abou-Samra AB. PTH and PTHrP signaling in osteoblasts. Cell. Signal. 21(8), 1245-1254 (2009).
24. Fiaschi-Taesch NM, Stewart AF. Minireview: Parathyroid hormone-related protein as an intracrine factor - Trafficking mechanisms and functional consequences. Endocrinology 144(2), 407-411 (2003).
25. Fidler IJ. The pathogenesis of cancer metastasis: The 'seed and soil' hypothesis revisited. Nat. Rev. Cancer 3(6), 453-458 (2003).
26. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 8(2), 98-101 (1889).
27. Steeg PS. Tumor metastasis: Mechanistic insights and clinical challenges. Nat. Med. 12(8), 895-904 (2006).
28. Southby J, Kissin MW, Danks JA et al. Immunohistochemical localization of parathyroid hormone-related protein in human breast cancer. Cancer Res. 50(23), 7710-7716 (1990).
29. Powell GJ, Southby J, Danks JA et al. Localization of parathyroid hormone-related protein in breast cancer metastases: Increased incidence in bone compared with other sites. Cancer Res. 51(11), 3059-3061 (1991).
30. Malakouti S, Asadi FK, Kukreja SC, Abcarian HA, Cintron JR. Parathyroid hormone-related protein expression in the human colon: Immunohistochemical evaluation. Am. Surg. 62(7), 540-544 (1996).
31. Shen X, Rychahou PG, Evers BM, Falzon M. PTHrP increases xenograft growth and promotes integrin alpha6beta4 expression and Akt activation in colon cancer. Cancer Lett. 258(2), 241-252 (2007).
32. Guise TA, Yin JJ, Taylor SD et al. Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J. Clin. Invest. 98(7), 1544-1549 (1996).
33. Iwamura M, di Sant'Agnese PA, Wu G et al. Immunohistochemical localization of parathyroid hormone-related protein in human prostate cancer. Cancer Res. 53(8), 1724-1726 (1993).
34. Montgrain PR, Deftos LJ, Arenberg D et al. Prognostic implications of parathyroid hormone-related protein in males and females with non-small-cell lung cancer. Clin. Lung Cancer 12(3), 197-205 (2011).
35. Henderson MA, Danks JA, Slavin JL et al. Parathyroid hormone-related protein localization in breast cancers predict improved prognosis. Cancer Res. 66(4), 2250-2256 (2006).
36. Ghoussaini M, Fletcher O, Michailidou K et al. Genome-wide association analysis identifies three new breast cancer susceptibility loci. Nat. Genet. 44(3), 312-318 (2012).
37. Dougherty KM, Blomme EA, Koh AJ et al. Parathyroid hormone-related protein as a growth regulator of prostate carcinoma. Cancer Res. 59(23), 6015-6022 (1999).
38. Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin. Cancer Res. 12(20 Pt 2), 6243s-6249s (2006).
39. Bubendorf L, Schopfer A, Wagner U et al. Metastatic patterns of prostate cancer: An autopsy study of 1,589 patients. Hum. Pathol. 31(5), 578-583 (2000).
40. Chiang AC, Massague J. Molecular basis of metastasis. N. Engl. J. Med. 359(26), 2814-2823 (2008).
41. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: A fatal attraction. Nat. Rev. Cancer 11(6), 411-425 (2011).
42. Loberg RD, Gayed BA, Olson KB, Pienta KJ. A paradigm for the treatment of prostate cancer bone metastases based on an understanding of tumor cell-microenvironment interactions. J. Cell. Biochem. 96(3), 439-446 (2005).
43. Chirgwin JM, Guise TA. Skeletal metastases: Decreasing tumor burden by targeting the bone microenvironment. J. Cell. Biochem. 102(6), 1333-1342 (2007).
44. Lam MH, Briggs LJ, Hu W, Martin TJ, Gillespie MT, Jans DA. Importin beta recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin alpha. J. Biol. Chem. 274(11), 7391-7398 (1999).
45. Lam MH, Thomas RJ, Loveland KL et al. Nuclear transport of parathyroid hormone (PTH)-related protein is dependent on microtubules. Mol. Endocrinol. 16(2), 390-401 (2002).
46. Watson PH, Fraher LJ, Hendy GN et al. Nuclear localization of the type 1 PTH/PTHrP receptor in rat tissues. J. Bone Miner. Res. 15(6), 1033-1044 (2000).
47. Watson PH, Fraher LJ, Natale BV, Kisiel M, Hendy GN, Hodsman AB. Nuclear localization of the type 1 parathyroid hormone/parathyroid hormone-related peptide receptor in MC3T3-E1 cells: Association with serum-induced cell proliferation. Bone 26(3), 221-225 (2000).
48. Nardozzi JD, Lott K, Cingolani G. Phosphorylation meets nuclear import: A review. Cell Commun. Signal. 8, 32 (2010).
49. Nguyen MT, Karaplis AC. The nucleus: A target site for parathyroid hormone-related peptide (PTHrP) action. J. Cell. Biochem. 70(2), 193-199 (1998).
50. Li J, Karaplis AC, Huang DC et al. PTHrP drives breast tumor initiation, progression, and metastasis in mice and is a potential therapy target. J. Clin. Invest. 121(12), 4655-4669 (2011).
51. Gujral A, Burton DW, Terkeltaub R, Deftos LJ. Parathyroid hormone-related protein induces interleukin 8 production by prostate cancer cells via a novel intracrine mechanism not mediated by its classical nuclear localization sequence. Cancer Res. 61(5), 2282-2288 (2001).
52. Burton PB, Moniz C, Knight DE. Parathyroid hormone related peptide can function as an autocrine growth factor in human renal cell carcinoma. Biochem. Biophys. Res. Commun. 167(3), 1134-1138 (1990).
53. Tovar Sepulveda VA, Shen X, Falzon M. Intracrine PTHrP protects against serum starvation-induced apoptosis and regulates the cell cycle in MCF-7 breast cancer cells. Endocrinology 143(2), 596-606 (2002).
54. Massfelder T, Lang H, Schordan E et al. Parathyroid hormone-related protein is an essential growth factor for human clear cell renal carcinoma and a target for the von Hippel-Lindau tumor suppressor gene. Cancer Res. 64(1), 180-188 (2004).
55. Talon I, Lindner V, Sourbier C et al. Antitumor effect of parathyroid hormone-related protein neutralizing antibody in human renal cell carcinoma in vitro and in vivo. Carcinogenesis 27(1), 73-83 (2006).
56. Shen X, Falzon M. Parathyroid hormone-related protein upregulates integrin expression via an intracrine pathway in PC-3 prostate cancer cells. Regul. Pept. 113(1-3), 17-29 (2003).
57. Shen X, Mula RV, Evers BM, Falzon M. Increased cell survival, migration, invasion, and Akt expression in PTHrP-overexpressing LoVo colon cancer cell lines. Regul. Pept. 141(1-3), 61-72 (2007).
58. Mula RV, Bhatia V, Falzon M. PTHrP promotes colon cancer cell migration and invasion in an integrin alpha6beta4- dependent manner through activation of Rac1. Cancer Lett. 298(1), 119-127 (2010).
59. Sakamoto S, Kyprianou N. Targeting anoikis resistance in prostate cancer metastasis. Mol. Aspects Med. 31(2), 205-214 (2010).
60. Bhatia V, Mula RV, Weigel NL, Falzon M. Parathyroid hormone-related protein regulates cell survival pathways via integrin alpha6beta4-mediated activation of phosphatidylinositol 3-kinase/Akt signaling. Mol. Cancer Res. 7(7), 1119-1131 (2009).
61. Park SI, McCauley LK. Nuclear localization of parathyroid hormone-related peptide confers resistance to anoikis in prostate cancer cells. Endocr. Relat. Cancer 19(3), 243-254 (2012).
62. Yin JJ, Selander K, Chirgwin JM et al. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J. Clin. Invest. 103(2), 197-206 (1999).
63. Li X, Loberg R, Liao J et al. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Cancer Res. 69(4), 1685-1692 (2009).
64. Rozel S, Galban CJ, Nicolay K et al. Synergy between anti-CCL2 and docetaxel as determined by DW-MRI in a metastatic bone cancer model. J. Cell. Biochem. 107(1), 58-64 (2009).
65. Mizutani K, Sud S, McGregor NA et al. The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia 11(11), 1235-1242 (2009).
66. Loberg RD, Ying C, Craig M et al. Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res. 67(19), 9417-9424 (2007).
67. Horwitz MJ, Tedesco MB, Sereika SM et al. A 7 day continuous infusion of PTH or PTHrP suppresses bone formation and uncouples bone turnover. J. Bone Miner. Res. 26(9), 2287-2297 (2011).
68. Datta NS, Chen C, Berry JE, McCauley LK. PTHrP signaling targets cyclin D1 and induces osteoblastic cell growth arrest. J. Bone Miner. Res. 20(6), 1051-1064 (2005).
69. Datta NS, Pettway GJ, Chen C, Koh AJ, McCauley LK. Cyclin D1 as a target for the proliferative effects of PTH and PTHrP in early osteoblastic cells. J. Bone Miner. Res. 22(7), 951-964 (2007).
70. Bonewald LF. The amazing osteocyte. J. Bone Miner. Res. 26(2), 229-238 (2011).
71. Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA. Matrix-embedded cells control osteoclast formation. Nat. Med. 17(10), 1235-1241 (2011).
72. Nakashima T, Hayashi M, Fukunaga T et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 17(10), 1231-1234 (2011).
73. Powell WF Jr, Barry KJ, Tulum I et al. Targeted ablation of the PTH/PTHrP receptor in osteocytes impairs bone structure and homeostatic calcemic responses. J. Endocrinol. 209(1), 21-32 (2011).
74. Sato K, Fujii Y, Kasono K et al. Parathyroid hormone-related protein and interleukin-1 alpha synergistically stimulate bone resorption in vitro and increase the serum calcium concentration in mice in vivo. Endocrinology 124(5), 2172-2178 (1989).
75. Uy HL, Mundy GR, Boyce BF et al. Tumor necrosis factor enhances parathyroid hormone-related protein-induced hypercalcemia and bone resorption without inhibiting bone formation in vivo. Cancer Res. 57(15), 3194-3199 (1997).
76. De La Mata J, Uy HL, Guise TA et al. Interleukin-6 enhances hypercalcemia and bone resorption mediated by parathyroid hormone-related protein in vivo. J. Clin. Invest. 95(6), 2846-2852 (1995).
77. Funk JL. A role for parathyroid hormone-related protein in the pathogenesis of inflammatory/autoimmune diseases. Int. Immunopharmacol. 1(6), 1101-1121 (2001).
78. Akino K, Ohtsuru A, Kanda K et al. Parathyroid hormone-related peptide is a potent tumor angiogenic factor. Endocrinology 141(11), 4313-4316 (2000).
79. Bakre MM, Zhu Y, Yin H et al. Parathyroid hormone-related peptide is a naturally occurring, protein kinase A-dependent angiogenesis inhibitor. Nat. Med. 8(9), 995-1003 (2002).
80. Liao J, Li X, Koh AJ et al. Tumor expressed PTHrP facilitates prostate cancer-induced osteoblastic lesions. Int. J. Cancer 123(10), 2267-2278 (2008).
81. Zhang J, Patel L, Pienta KJ. CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis. Cytokine Growth Factor Rev. 21(1), 41-48 (2010).
82. Roca H, Varsos ZS, Sud S, Craig MJ, Ying C, Pienta KJ. CCL2 and interleukin-6 promote survival of human CD11b+ peripheral blood mononuclear cells and induce M2-type macrophage polarization. J. Biol. Chem. 284(49), 34342-34354 (2009).
83. Cackowski FC, Anderson JL, Patrene KD et al. Osteoclasts are important for bone angiogenesis. Blood 115(1), 140-149 (2010).
84. Guise TA, Yin JJ, Thomas RJ, Dallas M, Cui Y, Gillespie MT. Parathyroid hormone-related protein (PTHrP)-(1-139) isoform is efficiently secreted in vitro and enhances breast cancer metastasis to bone in vivo. Bone 30(5), 670-676 (2002).
85. Onuma E, Azuma Y, Saito HM et al. Increased renal calcium reabsorption by parathyroid hormone-related protein is a causative factor in the development of humoral hypercalcemia of malignancy refractory to osteoclastic bone resorption inhibitors. Clin. Cancer Res. 11(11), 4198-4203 (2005).
86. Furugaki K, Moriya Y, Iwai T et al. Erlotinib inhibits osteolytic bone invasion of human non-small-cell lung cancer cell line NCI-H292. Clin. Exp. Metastasis 28(7), 649-659 (2011).
87. Lorch G, Gilmore JL, Koltz PF et al. Inhibition of epidermal growth factor receptor signalling reduces hypercalcaemia induced by human lung squamous-cell carcinoma in athymic mice. Br. J. Cancer 97(2), 183-193 (2007).
88. Kaplan RN, Psaila B, Lyden D. Bone marrow cells in the 'pre-metastatic niche': Within bone and beyond. Cancer Metastasis Rev. 25(4), 521-529 (2006).
89. Kaplan RN, Riba RD, Zacharoulis S et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438(7069), 820-827 (2005).
90. Hiratsuka S, Watanabe A, Sakurai Y et al. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 10(11), 1349-1355 (2008).
91. Hiratsuka S, Watanabe A, Aburatani H, Maru Y. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8(12), 1369-1375 (2006).
92. Kelly T, Suva LJ, Huang Y et al. Expression of heparanase by primary breast tumors promotes bone resorption in the absence of detectable bone metastases. Cancer Res. 65(13), 5778-5784 (2005).
93. Kelly T, Suva LJ, Nicks KM, MacLeod V, Sanderson RD. Tumor-derived syndecan-1 mediates distal cross-talk with bone that enhances osteoclastogenesis. J. Bone Miner. Res. 25(6), 1295-1304 (2010).
94. Anborgh PH, Mutrie JC, Tuck AB, Chambers AF. Role of the metastasis-promoting protein osteopontin in the tumour microenvironment. J. Cell. Mol. Med. 14(8), 2037-2044 (2010).
95. Lynch CC, Hikosaka A, Acuff HB et al. MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell 7(5), 485-496 (2005).
96. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4(1), 71-78 (2004).
97. Younos I, Donkor M, Hoke T et al. Tumor- and organ-dependent infiltration by myeloid-derived suppressor cells. Int. Immunopharmacol. 11(7), 816-826 (2011).
98. Yang L, Edwards CM, Mundy GR. Gr-1+CD11b+ myeloid-derived suppressor cells: Formidable partners in tumor metastasis. J. Bone Miner. Res. 25(8), 1701-1706 (2010).
99. Park SI, Sadler W, Koh AJ, Soki F, McCauley LK. Parathyroid hormone-related peptide (PTHrP) up-regulates myeloid-derived suppressor cells (MDSC) in the bone marrow, contributing to prostate cancer growth and angiogenesis. Presented at: AMERICAN Society for Bone and Mineral Research 2011 Annual Meeting. San Diego, CA, USA, 16-20 September 2011 (Abstract 1088).
100. Gao CL, Dean RC, Pinto A et al. Detection of circulating prostate specific antigen expressing prostatic cells in the bone marrow of radical prostatectomy patients by sensitive reverse transcriptase polymerase chain reaction. J. Urol. 161(4), 1070-1076 (1999).
101. Langley RR, Fidler IJ. The seed and soil hypothesis revisited - The role of tumor-stroma interactions in metastasis to different organs. Int. J. Cancer 128(11), 2527-2535 (2011).
102. Nguyen DX, Bos PD, Massague J. Metastasis: From dissemination to organ-specific colonization. Nat. Rev. Cancer 9(4), 274-284 (2009).