A prototypic matricellular protein in the tumor microenvironment - Where there's SPARC, there's fire

Journal of Cellular Biochemistry

Volumn 104, Issue 3, 2008, Pages 721-732

  Clark, Clancy J ^a   Sage, E Helene ^b  

^a VIRGINIA MASON MEDICAL CENTER   (United States)

^b BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

Angiogenesis; Desmoplasia; Matricellular protein; SPARC; Tumor microenvironment

Indexed keywords

CYTOKINE; GROWTH FACTOR; OSTEONECTIN; PROTEINASE;

ANGIOGENESIS; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL INTERACTION; DEVELOPMENT; EVOLUTION; EXTRACELLULAR MATRIX; GENOME ANALYSIS; HOMEOSTASIS; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TUMOR;

ANIMALS; CELL MOVEMENT; COMPUTATIONAL BIOLOGY; CYSTEINE; DISEASE PROGRESSION; EVOLUTION; GLYCOPROTEINS; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OSTEONECTIN; SYSTEMS BIOLOGY;

ANIMALIA; VERTEBRATA;

EID: 45149106189     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21688     Document Type: Review

References (112)

1. Aderem A. 2005. Systems biology: Its practice and challenges. Cell 121:511-513.
2. Albini A, Sporn MB. 2007. The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 7:139-147.
3. Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK. 2006. Physicochemical modelling of cell signalling pathways. Nat Cell Biol 8:1195-1203.
4. Allinen M, Beroukhim R, Cai L, Brennan C, Lahti-Domenici J, Huang H, Porter D, Hu M, Chin L, Richardson A, Schnitt S, Sellers WR, Polyak K. 2004. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 6:17-32.
5. Alvarez MJ, Prada F, Salvatierra E, Bravo AI, Lutzky VP, Carbone C, Pitossi FJ, Chuluyan HE, Podhajcer OL. 2005. Secreted protein acidic and rich in cysteine produced by human melanoma cells modulates polymorphonuclear leukocyte recruitment and antitumor cytotoxic capacity. Cancer Res 65:5123-5132.
6. Anderson AR, Weaver AM, Cummings PT, Quaranta V. 2006. Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127:905-915.
7. Aycock RL, Bradshaw AC, Sage EH, Starcher B. 2004. Development of UV-induced squamous cell carcinomas is suppressed in the absence of SPARC. J Invest Dermatol 123:592-599.
8. Barker TH, Framson P, Puolakkainen PA, Reed M, Funk SE, Sage EH. 2005. Matricellular homologs in the foreign body response: Hevin suppresses inflammation, but hevin and SPARC together diminish angiogenesis. Am J Pathol 166:923-933.
9. Bellahcène A, Castronovo V. 1995. Increased expression of osteonectin and osteopontin, two bone matrix proteins, in human breast cancer. Am J Pathol 146:95-100.
10. Bloomston M, Ellison EC, Muscarella P, Al-Saif O, Martin EW, Melvin WS, Frankel WL. 2007. Stromal osteonectin overexpression is associated with poor outcome in patients with ampullary cancer. Ann Surg Oncol 14:211-217.
11. Boon K, Osorio EC, Greenhut SF, Schaefer CF, Shoemaker J, Polyak K, Morin PJ, Buetow KH, Strausberg RL, De Souza SJ, Riggins GJ. 2002. An anatomy of normal and malignant gene expression. Proc Natl Acad Sci USA 99:11287-11292.
12. Bornstein P. 1995. Diversity of function is inherent in matricellular proteins: An appraisal of thrombospondin 1. J Cell Biol 130:503-506.
13. Bradshaw AD, Sage EH. 2001. SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107:1049-1054.
14. Bradshaw AD, Reed MJ, Carbon JG, Pinney E, Brekken RA, Sage EH. 2001. Increased fibrovascular invasion of subcutaneous polyvinyl alcohol sponges in SPARC-null mice. Wound Repair Regen 9:522-530.
15. Bradshaw AD, Reed MJ, Sage EH. 2002. SPARC-null mice exhibit accelerated cutaneous wound closure. J Histochem Cytochem 50:1-10.
16. Brekken RA, Puolakkainen P, Graves DC, Workman G, Lubkin SR, Sage EH. 2003. Enhanced growth of tumors in SPARC null mice is associated with changes in the ECM. J Clin Invest 111:487-495.
17. Buchman TG. 2002. The community of the self. Nature 420:246-251.
18. Che Y, Luo A, Wang H, Qi J, Guo J, Liu Z. 2006. The differential expression of SPARC in esophageal squamous cell carcinoma. Int J Mol Med 17:1027-1033.
19. Chin D, Boyle GM, Williams RM, Ferguson K, Pandeya N, Pedley J, Campbell CM, Theile DR, Parsons PG, Coman WB. 2005. Novel markers for poor prognosis in head and neck cancer. Int J Cancer 113:789-797.
20. Chlenski A, Liu S, Crawford SE, Volpert OV, DeVries GH, Evangelista A, Yang Q, Salwen HR, Farrer R, Bray J, Cohn SL. 2002. SPARC is a key Schwannian-derived inhibitor controlling neuroblastoma tumor angiogenesis. Cancer Res 62:7357-7363.
21. Chlenski A, Liu S, Baker LJ, Yang Q, Tian Y, Salwen HR, Cohn SL. 2004. Neuroblastoma angiogenesis is inhibited with a folded synthetic molecule corresponding to the epidermal growth factor-like module of the follistatin domain of SPARC. Cancer Res 64:7420-7425.
22. Chlenski A, Liu S, Guerrero LJ, Yang Q, Tian Y, Salwen HR, Zage P, Cohn SL. 2006. SPARC expression is associated with impaired tumor growth, inhibited angiogenesis and changes in the extracellular matrix. Int J Cancer 118:310-316.
23. Chu GC, Kimmelman AC, Hezel AF, DePinho RA. 2007. Stromal biology of pancreatic cancer. J Cell Biochem 101:887-907.
24. De S, Chen J, Narizhneva NV, Heston W, Brainard J, Sage EH, Byzova TV. 2003. Molecular pathway for cancer metastasis to bone. J Biol Chem 278:39044-39050.
25. De Vos J, Thykjaer T, Tarte K, Ensslen M, Raynaud P, Requirand G, Pellet F, Pantesco V, Rème T, Jourdan M, Rossi JF, Ørntoft T, Klein B. 2002. Comparison of gene expression profiling between malignant and normal plasma cells with oligonucleotide arrays. Oncogene 21:6848-6857.
26. Dvorak HF. 1986. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315:1650-1659.
27. Fanburg-Smith JC, Bratthauer GL, Miettinen M. 1999. Osteocalcin and osteonectin immunoreactivity in extra-skeletal osteosarcoma: A study of 28 cases. Hum Pathol 30:32-38.
28. Framson PE, Sage EH. 2004. SPARC and tumor growth: Where the seed meets the soil? J Cell Biochem 92:679-690.
29. Funk SE, Sage EH. 1993. Differential effects of SPARC and cationic SPARC peptides on DNA synthesis by endothelial cells and fibroblasts. J Cell Physiol 154:53-63.
30. Gilmour DT, Lyon GJ, Carlton MB, Sanes JR, Cunningham JM, Anderson JR, Hogan BL, Evans MJ, Colledge WH. 1998. Mice deficient for the secreted glycoprotein SPARC/osteonectin/BM40 develop normally but show severe age-onset cataract formation and disruption of the lens. EMBO J 17:1860-1870.
31. Goh KI, Cusick ME, Valle D, Childs B, Vidal M, Barabási AL. 2007. The human disease network. Proc Natl Acad Sci USA 104:8685-8690.
32. Guweidhi A, Kleeff J, Adwan H, Giese NA, Wente MN, Giese T, Büchler MW, Berger MR, Friess H. 2005. Osteonectin influences growth and invasion of pancreatic cancer cells. Ann Surg 242:224-234.
33. Hedvat CV, Comenzo RL, Teruya-Feldstein J, Olshen AB, Ely SA, Osman K, Zhang Y, Kalakonda N, Nimer SD. 2003. Insights into extramedullary tumour cell growth revealed by expression profiling of human plasmacytomas and multiple myeloma. Br J Haematol 122:728-744.
34. Hu M, Yao J, Cai L, Bachman KE, van den Brûle F, Velculescu V, Polyak K. 2005. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 37:899-905.
35. Iacobuzio-Donahue CA, Argani P, Hempen PM, Jones J, Kern SE. 2002. The desmoplastic response to infiltrating breast carcinoma: Gene expression at the site of primary invasion and implications for comparisons between tumor types. Cancer Res 62:5351-5357.
36. Infante JR, Matsubayashi H, Sato N, Tonascia J, Klein AP, Riall TA, Yeo C, Iacobuzio-Donahue C, Goggins M. 2007. Peritumoral fibroblast SPARC expression and patient outcome with resectable pancreatic adenocarcinoma. J Clin Oncol 25:319-325.
37. Jendraschak E, Sage EH. 1996. Regulation of angiogenesis by SPARC and angiostatin: Implications for tumor cell biology. Semin Cancer Biol 7:139-146.
38. Kalluri R, Zeisberg M. 2006. Fibroblasts in cancer. Nat Rev Cancer 6:392-401.
39. Karsenti E, Nédélec F, Surrey T. 2006. Modelling microtubule patterns. Nat Cell Biol 8:1204-1211.
40. Kato Y, Nagashima Y, Baba Y, Kawano T, Furukawa M, Kubota A, Yanoma S, Imagawa-Ishiguro Y, Satake K, Taguchi T, Hata R, Mochimatsu I, Aoki I, Kameda Y, Inayama Y, Tsukuda M. 2005. Expression of SPARC in tongue carcinoma of stage II is associated with poor prognosis: An immunohistochemical study of 86 cases. Int J Mol Med 16:263-268.
41. Kawasaki K, Suzuki T, Weiss KM. 2004. Genetic basis for the evolution of vertebrate mineralized tissue. Proc Natl Acad Sci USA 101:11356-11361.
42. Kelly KA, Waterman P, Weissleder R. 2006. In vivo imaging of molecularly targeted phage. Neoplasia 8:1011-1018.
43. Kelly KA, Allport JR, Yu AM, Sinh S, Sage EH, Gerszten RE, Weissleder R. 2007. SPARC is a VCAM-1 counter-ligand that mediates leukocyte transmigration. J Leukoc Biol 81:748-756.
44. Kitano H. 2002. Computational systems biology. Nature 420:206-210.
45. Koukourakis MI, Giatromanolaki A, Brekken RA, Sivridis E, Gatter KC, Harris AL, Sage EH. 2003. Enhanced expression of SPARC/osteonectin in the tumor-associated stroma of non-small cell lung cancer is correlated with markers of hypoxia/acidity and with poor prognosis of patients. Cancer Res 63:5376-5380.
46. Kzhyshkowska J, Workman G, Cardó-Vila M, Arap W, Pasqualini R, Gratchev A, Krusell L, Goerdt S, Sage EH. 2006. Novel function of alternatively activated macrophages: Stabilin-1-mediated clearance of SPARC. J Immunol 176:5825-5832.
47. Lane TF, Sage EH. 1994. The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J 8:163-173.
48. Lane TF, Iruela-Arispe ML, Johnson RS, Sage EH. 1994. SPARC is a source of copper-binding peptides that stimulate angiogenesis. J Cell Biol 125:929-943.
49. Lau CP, Poon RT, Cheung ST, Yu WC, Fan ST. 2006. SPARC and Hevin expression correlate with tumour angiogenesis in hepatocellular carcinoma. J Pathol 210:459-468.
50. Le Bail B, Faouzi S, Boussarie L, Guirouilh J, Blanc JF, Carles J, Bioulac-Sage P, Balabaud C, Rosenbaum J. 1999. Osteonectin/SPARC is overexpressed in human hepatocellular carcinoma. J Pathol 189:46-52.
51. Ledda F, Bravo AI, Adris S, Bover L, Mordoh J, Podhajcer OL. 1997a. The expression of the secreted protein acidic and rich in cysteine (SPARC) is associated with the neoplastic progression of human melanoma. J Invest Dermatol 108:210-214.
52. Ledda MF, Adris S, Bravo AI, Kairiyama C, Bover L, Chernajovsky Y, Mordoh J, Podhajcer OL. 1997b. Suppression of SPARC expression by antisense RNA abrogates the tumorigenicity of human melanoma cells. Nat Med 3:171-176.
53. Lewandoski M. 2001. Conditional control of gene expression in the mouse. Nat Rev Genet 2:743-755.
54. Li H, Fan X, Houghton J. 2007. Tumor microenvironment: The role of the tumor stroma in cancer. J Cell Biochem 101:805-815.
55. Lien HC, Hsiao YH, Lin YS, Yao YT, Juan HF, Kuo WH, Hung MC, Chang KJ, Hsieh FJ. 2007. Molecular signatures of metaplastic carcinoma of the breast by large-scale transcriptional profiling: Identification of genes potentially related to epithelial-mesenchymal transition. Oncogene 26:7859-7871.
56. Lopez MV, Blanco P, Viale DL, Cafferata EG, Carbone C, Gould D, Chernajovsky Y, Podhajcer OL. 2006. Expression of a suicidal gene under control of the human secreted protein acidic and rich in cysteine (SPARC) promoter in tumor or stromal cells led to the inhibition of tumor cell growth. Mol Cancer Ther 5:2503-2511.
57. Luo A, Kong J, Hu G, Liew CC, Xiong M, Wang X, Ji J, Wang T, Zhi H, Wu M, Liu Z. 2004. Discovery of Ca2+-relevant and differentiation-associated genes downregulated in esophageal squamous cell carcinoma using cDNA microarray. Oncogene 23:1291-1299.
58. Lussier C, Sodek J, Beaulieu JF. 2001. Expression of SPARC/osteonectin/ BM40 in the human gut: Predominance in the stroma of the remodeling distal intestine. J Cell Biochem 81:463-476.
59. Maeng HY, Song SB, Choi DK, Kim KE, Jeong HY, Sakaki Y, Furihata C. 2002. Osteonectin-expressing cells in human stomach cancer and their possible clinical significance. Cancer Lett 184:117-121.
60. Mason IJ, Taylor A, Williams JG, Sage H, Hogan BL. 1986. Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell 'culture shock' glycoprotein of Mr 43,000. EMBO J 5:1465-1472.
61. Massi D, Franchi A, Borgognoni L, Reali UM, Santucci M. 1999. Osteonectin expression correlates with clinical outcome in thin cutaneous malignant melanomas. Hum Pathol 30:339-344.
62. Motamed K. 1999. SPARC (osteonectin/BM-40). Int J Biochem Cell Biol 31:1363-1366.
63. Ng KW, Manji SS, Young MF, Findlay DM. 1989. Opposing influences of glucocorticoid and retinoic acid on transcriptional control in preosteoblasts. Mol Endocrinol 3:2079-2085.
64. Nomura S, Hashmi S, McVey JH, Ham J, Parker M, Hogan BL. 1989. Evidence for positive and negative regulatory elements in the 5′-flanking sequence of the mouse spare (osteonectin) gene. J Biol Chem 264:12201-12207.
65. Norose K, Clark JI, Syed NA, Basu A, Heber-Katz E, Sage EH, Howe CC. 1998. SPARC deficiency leads to early-onset cataractogenesis. Invest Ophthalmol Vis Sci 39:2674-2680.
66. Nozaki M, Sakurai E, Raisler BJ, Baffi JZ, Witta J, Ogura Y, Brekken RA, Sage EH, Ambati BK, Ambati J. 2006. Loss of SPARC-mediated VEGFR-1 suppression after injury reveals a novel antiangiogenic activity of VEGF-A. J Clin Invest 116:422-429.
67. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. 1999. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59:5002-5011.
68. Paley PJ, Goff BA, Gown AM, Greer BE, Sage EH. 2000. Alterations in SPARC and VEGF immunoreactivity in epithelial ovarian cancer. Gynecol Oncol 78:336-341.
69. Parker BS, Argani P, Cook BP, Liangfeng H, Chartrand SD, Zhang M, Saha S, Bardelli A, Jiang Y, St Martin TB, Nacht M, Teicher BA, Klinger KW, Sukumar S, Madden SL. 2004. Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res 64:7857-7866.
70. Pen A, Moreno MJ, Martin J, Stanimirovic DB. 2007. Molecular markers of extracellular matrix remodeling in glioblastoma vessels: Microarray study of laser-captured glioblastoma vessels. Glia 55:559-572.
71. Porte H, Chastre E, Prevot S, Nordlinger B, Empereur S, Basset P, Chambon P, Gespach C. 1995. Neoplastic progression of human colorectal cancer is associated with overexpression of the stromelysin-3 and BM-40/SPARC genes. Int J Cancer 64:70-75.
72. Porte H, Triboulet JP, Kotelevets L, Carrat F, Prévot S, Nordlinger B, DiGioia Y, Wurtz A, Comoglio P, Gespach C, Chastre E. 1998. Overexpression of stromelysin-3, BM-40/SPARC, and MET genes in human esophageal carcinoma: Implications for prognosis. Clin Cancer Res 4:1375-1382.
73. Porter PL, Sage EH, Lane TF, Funk SE, Gown AM. 1995. Distribution of SPARC in normal and neoplastic human tissue. J Histochem Cytochem 43:791-800.
74. Porter DA, Krop IE, Nasser S, Sgroi D, Kaelin CM, Marks JR, Riggins G, Polyak K. 2001. A SAGE (serial analysis of gene expression) view of breast tumor progression. Cancer Res 61:5697-5702.
75. Potter JD. 2007. Morphogens, morphostats, microarchitecture and malignancy. Nat Rev Cancer 7:464-474.
76. Puolakkainen P, Reed M, Vento P, Sage EH, Kiviluoto T, Kivilaakso E. 1999. Expression of SPARC (secreted protein, acidic and rich in cysteine) in healing intestinal anastomoses and short bowel syndrome in rats. Dig Dis Sci 44:1554-1564.
77. Puolakkainen PA, Brekken RA, Muneer S, Sage EH. 2004. Enhanced growth of pancreatic tumors in SPARC-null mice is associated with decreased deposition of extracellular matrix and reduced tumor cell apoptosis. Mol Cancer Res 2:215-224.
78. Purcell L, Gruia-Gray J, Scanga S, Ringuette M. 1993. Developmental anomalies of Xenopus embryos following microinjection of SPARC antibodies. J Exp Zool 265:153-164.
79. Reed MJ, Sage EH. 1996. SPARC and the extracellular matrix: Implications for cancer and wound repair. Curr Top Microbiol Immunol 213(Pt 1):81-94.
80. Reed MJ, Bradshaw AD, Shaw M, Sadoun E, Han N, Ferara N, Funk S, Puolakkainen P, Sage EH. 2005. Enhanced angiogenesis characteristic of SPARC-null mice disappears with age. J Cell Physiol 204:800-807.
81. Rempel SA, Ge S, Gutiérrez JA. 1999. SPARC: A potential diagnostic marker of invasive meningiomas. Clin Cancer Res 5:237-241.
82. Rich JN, Shi Q, Hjelmeland M, Cummings TJ, Kuan CT, Bigner DD, Counter CM, Wang XF. 2003. Bone-related genes expressed in advanced malignancies induce invasion and metastasis in a genetically defined human cancer model. J Biol Chem 278:15951-15957.
83. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK, Dobra A, Dressman HK, Bigner DD, Nevins JR, West M. 2005. Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 65:4051-4058.
84. Robert G, Gaggioli C, Bailet O, Chavey C, Abbe P, Aberdam E, Sabatié E, Cano A, Garcia de Herreros A, Ballotti R, Tartare-Deckert S. 2006. SPARC represses E-cadherin and induces mesenchymal transition during melanoma development. Cancer Res 66:7516-7523.
85. Ruiter D, Bogenrieder T, Elder D, Herlyn M. 2002. Melanoma-stroma interactions: Structural and functional aspects. Lancet Oncol 3:35-43.
86. Sage EH. 1992. Modulation of endothelial cell shape by SPARC does not involve chelation of extracellular Ca2+ and Mg2+. Biochem Cell Biol 70:56-62.
87. Sage EH, Bornstein P. 1991. Extracellular proteins that modulate cell-matrix interactions. SPARC, tenascin, and thrombospondin. J Biol Chem 266:14831-14834.
88. Sage H, Johnson C, Bornstein P. 1984. Characterization of a novel serum albumin-binding glycoprotein secreted by endothelial cells in culture. J Biol Chem 259:3993-4007.
89. Sage H, Tupper J, Bramson R. 1986. Endothelial cell injury in vitro is associated with increased secretion of an Mr 43,000 glycoprotein ligand. J Cell Physiol 127:373-387.
90. Sage EH, Reed M, Funk SE, Truong T, Steadele M, Puolakkainen P, Maurice DH, Bassuk JA. 2003. Cleavage of the matricellular protein SPARC by matrix metalloproteinase 3 produces polypeptides that influence angiogenesis. J Biol Chem 278:37849-37857.
91. Sakai N, Baba M, Nagasima Y, Kato Y, Hirai K, Kondo K, Kobayashi K, Yoshida M, Kaneko S, Kishida T, Kawakami S, Hosaka M, Inayama Y, Yao M. 2001. SPARC expression in primary human renal cell carcinoma: Upregulation of SPARC in sarcomatoid renal carcinoma. Hum Pathol 32:1064-1070.
92. Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR, Colombo MP. 2003. Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 198:1475-1485.
93. Sansom OJ, Mansergh F, Evans M, Wilkins J, Clarke A. 2007. Deficiency of SPARC suppresses intestinal tumourigenesis in APCMin/+ Mice. Gut 56:1410-1414.
94. Schittenhelm J, Mittelbronn M, Roser F, Tatagiba M, Mawrin C, Bornemann A. 2006. Patterns of SPARC expression and basement membrane intactness at the tumour-brain border of invasive meningiomas. Neuropathol Appl Neurobiol 32:525-531.
95. Schneider S, Yochim J, Brabender J, Uchida K, Danenberg KD, Metzger R, Schneider PM, Salonga D, Hölscher AH, Danenberg PV. 2004. Osteopontin but not osteonectin messenger RNA expression is a prognostic marker in curatively resected non-small cell lung cancer. Clin Cancer Res 10:1588-1596.
96. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA. 2002. Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 62:6270-6277.
97. Schulz A, Jundt G, Berghäuser KH, Gehron-Robey P, Termine JD. 1988. Immunohistochemical study of osteonectin in various types of osteosarcoma. Am J Pathol 132:233-238.
98. Schwarzbauer JE, Spencer CS. 1993. The Caenorhabditis elegans homologue of the extracellular calcium binding protein SPARC/osteonectin affects nematode body morphology and mobility. Mol Biol Cell 4:941-952.
99. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, Kinzler KW. 2000. Genes expressed in human tumor endothelium. Science 289:1197-1202.
100. Takano T, Hasegawa Y, Miyauchi A, Matsuzuka F, Yoshida H, Kuma K, Hayashi N, Nakamori S, Amino N. 2002. Quantitative analysis of osteonectin mRNA in thyroid carcinomas. Endocr J 49:511-516.
101. Tanaka S, Nambu F, Nambu Z. 2001. Isolation of a cDNA encoding a putative SPARC from the brine shrimp, Artemia franciscana. Gene 268:53-58.
102. Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML, Martin GR. 1981. Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26:99-105.
103. Thomas R, True LD, Bassuk JA, Lange PH, Vessella RL. 2000. Differential expression of osteonectin/SPARC during human prostate cancer progression. Clin Cancer Res 6:1140-1149.
104. Turk N, Kusec R, Jaksic B, Turk Z. 2005. Humoral SPARC/osteonectin protein in plasma cell dyscrasias. Ann Hematol 84:304-310.
105. Wang CS, Lin KH, Chen SL, Chan YF, Hsueh S. 2004. Overexpression of SPARC gene in human gastric carcinoma and its clinic-pathologic significance. Br J Cancer 91:1924-1930.
106. Wewer UM, Albrechtsen R, Fisher LW, Young MF, Termine JD. 1988. Osteonectin/SPARC/BM-40 in human decidua and carcinoma, tissues characterized by de novo formation of basement membrane. Am J Pathol 132:345-355.
107. Witz IP, Levy-Nissenbaum O. 2006. The tumor microenvironment in the post-PAGET era. Cancer Lett 242:1-10.
108. Xue LY, Hu N, Song YM, Zou SM, Shou JZ, Qian LX, Ren LQ, Lin DM, Tong T, He ZG, Zhan QM, Taylor PR, Lu N. 2006. Tissue microarray analysis reveals a tight correlation between protein expression pattern and progression of esophageal squamous cell carcinoma. BMC Cancer 6:296.
109. Yamanaka M, Kanda K, Li NC, Fukumori T, Oka N, Kanayama HO, Kagawa S. 2001. Analysis of the gene expression of SPARC and its prognostic value for bladder cancer. J Urol 166:2495-2499.
110. Yamashita K, Upadhay S, Mimori K, Inoue H, Mori M. 2003. Clinical significance of secreted protein acidic and rich in cystein in esophageal carcinoma and its relation to carcinoma progression. Cancer 97:2412-2419.
111. Yan Q, Sage EH. 1999. SPARC, a matricellular glycoprotein with important biological functions. J Histochem Cytochem 47:1495-1506.
112. Yiu GK, Chan WY, Ng SW, Chan PS, Cheung KK, Berkowitz RS, Mok SC. 2001. SPARC (secreted protein acidic and rich in cysteine) induces apoptosis in ovarian cancer cells. Am J Pathol 159:609-622.