Collagen XVIII in tissue homeostasis and dysregulation — Lessons learned from model organisms and human patients

Matrix Biology

Volumn 57-58, Issue , 2017, Pages 55-75

  Heljasvaara, Ritva ^a,b   Aikio, Mari ^c   Ruotsalainen, Heli ^a   Pihlajaniemi, Taina ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF BERGEN   (Norway)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Basement membrane; Heparan sulphate proteoglycan; Knobloch syndrome; Multiplexin

Indexed keywords

COLLAGEN TYPE 18; ENDOSTATIN; FRIZZLED PROTEIN; PROTEOGLYCAN; RECOMBINANT ENDOSTATIN; THROMBOSPONDIN 1; COL18A1 PROTEIN, HUMAN; COLLAGEN TYPE 8; ISOPROTEIN; RECOMBINANT PROTEIN;

ADIPOGENESIS; ANGIOGENESIS; BONE MARROW; CANCER GROWTH; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; ENCEPHALOCELE; ENDOTHELIUM CELL; EYE MALFORMATION; GENE MUTATION; GENE STRUCTURE; GENETIC DISORDER; HOMEOSTASIS; HUMAN; KIDNEY DEVELOPMENT; KIDNEY FIBROSIS; KNOBLOCH SYNDROME; LIPID STORAGE; NEPHRITIS; NERVOUS SYSTEM; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; RARE DISEASE; REVIEW; STEM CELL; ANIMAL; BASEMENT MEMBRANE; CELL MOTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PROTEIN DEGRADATION; PROTEIN DOMAIN; RETINA DETACHMENT;

ANIMALS; BASEMENT MEMBRANE; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN TYPE VIII; ENCEPHALOCELE; ENDOSTATINS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN DOMAINS; PROTEIN ISOFORMS; PROTEOLYSIS; RECOMBINANT PROTEINS; RETINAL DETACHMENT;

EID: 85006166351     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2016.10.002     Document Type: Review

References (185)

1. [1] Saarela, J., Rehn, M., Oikarinen, A., Autio-Harmainen, H., Pihlajaniemi, T., The short and long forms of type XVIII collagen show clear tissue specificities in their expression and location in basement membrane zones in humans. Am. J. Pathol. 153 (1998), 611–626.
2. [2] Halfter, W., Dong, S., Schurer, B., Cole, G.J., Collagen XVIII is a basement membrane heparan sulfate proteoglycan. J. Biol. Chem. 273 (1998), 25404–25412.
3. [3] Muragaki, Y., Timmons, S., Griffith, C.M., Oh, S.P., Fadel, B., Quertermous, T., Olsen, B.R., Mouse Col18a1 is expressed in a tissue-specific manner as three alternative variants and is localized in basement membrane zones. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 8763–8767.
4. [4] Miosge, N., Simniok, T., Sprysch, P., Herken, R., The collagen type XVIII endostatin domain is co-localized with perlecan in basement membranes in vivo. J. Histochem. Cytochem. 51 (2003), 285–296.
5. [5] Rehn, M., Pihlajaniemi, T., Identification of three N-terminal ends of type XVIII collagen chains and tissue-specific differences in the expression of the corresponding transcripts. The longest form contains a novel motif homologous to rat and Drosophila frizzled proteins. J. Biol. Chem. 270 (1995), 4705–4711.
6. [6] Oh, S.P., Kamagata, Y., Muragaki, Y., Timmons, S., Ooshima, A., Olsen, B.R., Isolation and sequencing of cDNAs for proteins with multiple domains of Gly-Xaa-Yaa repeats identify a distinct family of collagenous proteins. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 4229–4233.
7. [7] Myllyharju, J., Kivirikko, K.I., Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20 (2004), 33–43.
8. [8] Rehn, M., Pihlajaniemi, T., Alpha 1(XVIII), a collagen chain with frequent interruptions in the collagenous sequence, a distinct tissue distribution, and homology with type XV collagen. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 4234–4238.
9. [9] Muragaki, Y., Abe, N., Ninomiya, Y., Olsen, B.R., Ooshima, A., The human alpha 1(XV) collagen chain contains a large amino-terminal non-triple helical domain with a tandem repeat structure and homology to alpha 1(XVIII) collagen. J. Biol. Chem. 269 (1994), 4042–4046.
10. [10] Ackley, B.D., Crew, J.R., Elamaa, H., Pihlajaniemi, T., Kuo, C.J., Kramer, J.M., The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J. Cell Biol. 152 (2001), 1219–1232.
11. [11] Haftek, Z., Morvan-Dubois, G., Thisse, B., Thisse, C., Garrone, R., Le Guellec, D., Sequence and embryonic expression of collagen XVIII NC1 domain (endostatin) in the zebrafish. Gene Expr. Patterns 3 (2003), 351–354.
12. [12] Elamaa, H., Peterson, J., Pihlajaniemi, T., Destree, O., Cloning of three variants of type XVIII collagen and their expression patterns during Xenopus laevis development. Mech. Dev. 114 (2002), 109–113.
13. [13] Passos-Bueno, M.R., Suzuki, O.T., Armelin-Correa, L.M., Sertie, A.L., Errera, F.I., Bagatini, K., Kok, F., Leite, K.R., Mutations in collagen 18A1 and their relevance to the human phenotype. An. Acad. Bras. Cienc. 78 (2006), 123–131.
14. [14] Caglayan, A.O., Baranoski, J.F., Aktar, F., Han, W., Tuysuz, B., Guzel, A., Guclu, B., Kaymakcalan, H., Aktekin, B., Akgumus, G.T., Murray, P.B., Erson-Omay, E.Z., Caglar, C., Bakircioglu, M., Sakalar, Y.B., Guzel, E., Demir, N., Tuncer, O., Senturk, S., Ekici, B., Minja, F.J., Sestan, N., Yasuno, K., Bilguvar, K., Caksen, H., Gunel, M., Brain malformations associated with Knobloch syndrome—review of literature, expanding clinical spectrum, and identification of novel mutations. Pediatr. Neurol. 51 (2014), 806–813, e8.
15. [15] Suzuki, O., Kague, E., Bagatini, K., Tu, H., Heljasvaara, R., Carvalhaes, L., Gava, E., de Oliveira, G., Godoi, P., Oliva, G., Kitten, G., Pihlajaniemi, T., Passos-Bueno, M.R., Novel pathogenic mutations and skin biopsy analysis in Knobloch syndrome. Mol. Vis. 15 (2009), 801–809.
16. [16] Suzuki, O.T., Sertie, A.L., Der Kaloustian, V.M., Kok, F., Carpenter, M., Murray, J., Czeizel, A.E., Kliemann, S.E., Rosemberg, S., Monteiro, M., Olsen, B.R., Passos-Bueno, M.R., Molecular analysis of collagen XVIII reveals novel mutations, presence of a third isoform, and possible genetic heterogeneity in Knobloch syndrome. Am. J. Hum. Genet. 71 (2002), 1320–1329.
17. [17] Elamaa, H., Snellman, A., Rehn, M., Autio-Harmainen, H., Pihlajaniemi, T., Characterization of the human type XVIII collagen gene and proteolytic processing and tissue location of the variant containing a frizzled motif. Matrix Biol. 22 (2003), 427–442.
18. [18] Hohenester, E., Engel, J., Domain structure and organisation in extracellular matrix proteins. Matrix Biol. 21 (2002), 115–128.
19. [19] Sarrazin, S., Lamanna, W.C., Esko, J.D., Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol., 3, 2011, 10.1101/cshperspect.a004952.
20. [20] Celie, J.W., Keuning, E.D., Beelen, R.H., Drager, A.M., Zweegman, S., Kessler, F.L., Soininen, R., van den Born, J., Identification of L-selectin binding heparan sulfates attached to collagen type XVIII. J. Biol. Chem. 280 (2005), 26965–26973.
21. [21] Kawashima, H., Watanabe, N., Hirose, M., Sun, X., Atarashi, K., Kimura, T., Shikata, K., Matsuda, M., Ogawa, D., Heljasvaara, R., Rehn, M., Pihlajaniemi, T., Miyasaka, M., Collagen XVIII, a basement membrane heparan sulfate proteoglycan, interacts with L-selectin and monocyte chemoattractant protein-1. J. Biol. Chem. 278 (2003), 13069–13076.
22. [22] Folkman, J., Antiangiogenesis in cancer therapy—endostatin and its mechanisms of action. Exp. Cell Res. 312 (2006), 594–607.
23. [23] O'Reilly, M.S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W.S., Flynn, E., Birkhead, J.R., Olsen, B.R., Folkman, J., Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88 (1997), 277–285.
24. [24] Ramchandran, R., Dhanabal, M., Volk, R., Waterman, M.J., Segal, M., Lu, H., Knebelmann, B., Sukhatme, V.P., Antiangiogenic activity of restin, NC10 domain of human collagen XV: comparison to endostatin. Biochem. Biophys. Res. Commun. 255 (1999), 735–739.
25. [25] Fu, Y., Tang, H., Huang, Y., Song, N., Luo, Y., Unraveling the mysteries of endostatin. IUBMB Life 61 (2009), 613–626.
26. [26] Poluzzi, C., Iozzo, R.V., Schaefer, L., Endostatin and endorepellin: a common route of action for similar angiostatic cancer avengers. Adv. Drug Deliv. Rev. 97 (2016), 156–173.
27. [27] Ricard-Blum, S., Salza, R., Matricryptins and matrikines: biologically active fragments of the extracellular matrix. Exp. Dermatol. 23 (2014), 457–463.
28. [28] Walia, A., Yang, J.F., Huang, Y.H., Rosenblatt, M.I., Chang, J.H., Azar, D.T., Endostatin's emerging roles in angiogenesis, lymphangiogenesis, disease, and clinical applications. Biochim. Biophys. Acta 1850 (2015), 2422–2438.
29. [29] Nguyen, T.M., Subramanian, I.V., Xiao, X., Ghosh, G., Nguyen, P., Kelekar, A., Ramakrishnan, S., Endostatin induces autophagy in endothelial cells by modulating Beclin 1 and beta-catenin levels. J. Cell. Mol. Med. 13 (2009), 3687–3698.
30. [30] Chau, Y.P., Lin, S.Y., Chen, J.H., Tai, M.H., Endostatin induces autophagic cell death in EAhy926 human endothelial cells. Histol. Histopathol. 18 (2003), 715–726.
31. [31] Yamaguchi, Y., Takihara, T., Chambers, R.A., Veraldi, K.L., Larregina, A.T., Feghali-Bostwick, C.A., A peptide derived from endostatin ameliorates organ fibrosis. Sci. Transl. Med., 4, 2012, 136ra71.
32. [32] Wan, Y.Y., Tian, G.Y., Guo, H.S., Kang, Y.M., Yao, Z.H., Li, X.L., Liu, Q.H., Lin, D.J., Endostatin, an angiogenesis inhibitor, ameliorates bleomycin-induced pulmonary fibrosis in rats. Respir. Res., 14, 2013 (56-9921-14-56).
33. [33] Lin, C.H., Chen, J., Ziman, B., Marshall, S., Maizel, J., Goligorsky, M.S., Endostatin and kidney fibrosis in aging: a case for antagonistic pleiotropy?. Am. J. Physiol. Heart Circ. Physiol. 306 (2014), H1692–H1699.
34. [34] Lin, C.H., Chen, J., Zhang, Z., Johnson, G.V., Cooper, A.J., Feola, J., Bank, A., Shein, J., Ruotsalainen, H.J., Pihlajaniemi, T.A., Goligorsky, M.S., Endostatin and transglutaminase 2 are involved in fibrosis of the aging kidney. Kidney Int. 89 (2016), 1281–1292.
35. [35] Su, J., Stenbjorn, R.S., Gorse, K., Su, K., Hauser, K.F., Ricard-Blum, S., Pihlajaniemi, T., Fox, M.A., Target-derived matricryptins organize cerebellar synapse formation through alpha3beta1 integrins. Cell Rep. 2 (2012), 223–230.
36. [36] Zaferani, A., Talsma, D.T., Yazdani, S., Celie, J.W., Aikio, M., Heljasvaara, R., Navis, G.J., Pihlajaniemi, T., van den Born, J., Basement membrane zone collagens XV and XVIII/proteoglycans mediate leukocyte influx in renal ischemia/reperfusion. PLoS One, 9, 2014, e106732.
37. [37] Aikio, M., Elamaa, H., Vicente, D., Izzi, V., Kaur, I., Seppinen, L., Speedy, H.E., Kaminska, D., Kuusisto, S., Sormunen, R., Heljasvaara, R., Jones, E.L., Muilu, M., Jauhiainen, M., Pihlajamaki, J., Savolainen, M.J., Shoulders, C.C., Pihlajaniemi, T., Specific collagen XVIII isoforms promote adipose tissue accrual via mechanisms determining adipocyte number and affect fat deposition. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), E3043–E3052.
38. [38] Tomono, Y., Naito, I., Ando, K., Yonezawa, T., Sado, Y., Hirakawa, S., Arata, J., Okigaki, T., Ninomiya, Y., Epitope-defined monoclonal antibodies against multiplexin collagens demonstrate that type XV and XVIII collagens are expressed in specialized basement membranes. Cell Struct. Funct. 27 (2002), 9–20.
39. [39] Aikio, M., Hurskainen, M., Brideau, G., Hagg, P., Sormunen, R., Heljasvaara, R., Gould, D.B., Pihlajaniemi, T., Collagen XVIII short isoform is critical for retinal vascularization, and overexpression of the Tsp-1 domain affects eye growth and cataract formation. Invest. Ophthalmol. Vis. Sci. 54 (2013), 7450–7462.
40. [40] Kinnunen, A.I., Sormunen, R., Elamaa, H., Seppinen, L., Miller, R.T., Ninomiya, Y., Janmey, P.A., Pihlajaniemi, T., Lack of collagen XVIII long isoforms affects kidney podocytes, whereas the short form is needed in the proximal tubular basement membrane. J. Biol. Chem. 286 (2011), 7755–7764.
41. [41] Quelard, D., Lavergne, E., Hendaoui, I., Elamaa, H., Tiirola, U., Heljasvaara, R., Pihlajaniemi, T., Clement, B., Musso, O., A cryptic frizzled module in cell surface collagen 18 inhibits Wnt/beta-catenin signaling. PLoS One, 3, 2008, e1878.
42. [42] Sund, M., Kalluri, R., Tumor stroma derived biomarkers in cancer. Cancer Metastasis Rev. 28 (2009), 177–183.
43. [43] Oh, S.P., Warman, M.L., Seldin, M.F., Cheng, S.D., Knoll, J.H., Timmons, S., Olsen, B.R., Cloning of cDNA and genomic DNA encoding human type XVIII collagen and localization of the alpha 1(XVIII) collagen gene to mouse chromosome 10 and human chromosome 21. Genomics 19 (1994), 494–499.
44. [44] Rehn, M., Hintikka, E., Pihlajaniemi, T., Characterization of the mouse gene for the alpha 1 chain of type XVIII collagen (Col18a1) reveals that the three variant N-terminal polypeptide forms are transcribed from two widely separated promoters. Genomics 32 (1996), 436–446.
45. [45] Saarela, J., Ylikarppa, R., Rehn, M., Purmonen, S., Pihlajaniemi, T., Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts. Matrix Biol. 16 (1998), 319–328.
46. [46] Heljasvaara, R., Nyberg, P., Luostarinen, J., Parikka, M., Heikkila, P., Rehn, M., Sorsa, T., Salo, T., Pihlajaniemi, T., Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp. Cell Res. 307 (2005), 292–304.
47. [47] Musso, O., Rehn, M., Saarela, J., Theret, N., Lietard, J., Hintikka, Lotrian, D., Campion, J.P., Pihlajaniemi, T., Clement, B., Collagen XVIII is localized in sinusoids and basement membrane zones and expressed by hepatocytes and activated stellate cells in fibrotic human liver. Hepatology 28 (1998), 98–107.
48. [48] Sasaki, T., Fukai, N., Mann, K., Gohring, W., Olsen, B.R., Timpl, R., Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J. 17 (1998), 4249–4256.
49. [49] Wen, W., Moses, M.A., Wiederschain, D., Arbiser, J.L., Folkman, J., The generation of endostatin is mediated by elastase. Cancer Res. 59 (1999), 6052–6056.
50. [50] Ferreras, M., Felbor, U., Lenhard, T., Olsen, B.R., Delaisse, J., Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett. 486 (2000), 247–251.
51. [51] Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., Mothes, W., Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19 (2000), 1187–1194.
52. [52] Lin, H.C., Chang, J.H., Jain, S., Gabison, E.E., Kure, T., Kato, T., Fukai, N., Azar, D.T., Matrilysin cleavage of corneal collagen type XVIII NC1 domain and generation of a 28-kDa fragment. Invest. Ophthalmol. Vis. Sci. 42 (2001), 2517–2524.
53. [53] Boudko, S.P., Sasaki, T., Engel, J., Lerch, T.F., Nix, J., Chapman, M.S., Bachinger, H.P., Crystal structure of human collagen XVIII trimerization domain: a novel collagen trimerization fold. J. Mol. Biol. 392 (2009), 787–802.
54. [54] Ding, Y.H., Javaherian, K., Lo, K.M., Chopra, R., Boehm, T., Lanciotti, J., Harris, B.A., Li, Y., Shapiro, R., Hohenester, E., Timpl, R., Folkman, J., Wiley, D.C., Zinc-dependent dimers observed in crystals of human endostatin. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 10443–10448.
55. [55] Hohenester, E., Sasaki, T., Olsen, B.R., Timpl, R., Crystal structure of the angiogenesis inhibitor endostatin at 1.5 A resolution. EMBO J. 17 (1998), 1656–1664.
56. [56] Marneros, A.G., Keene, D.R., Hansen, U., Fukai, N., Moulton, K., Goletz, P.L., Moiseyev, G., Pawlyk, B.S., Halfter, W., Dong, S., Shibata, M., Li, T., Crouch, R.K., Bruckner, P., Olsen, B.R., Collagen XVIII/endostatin is essential for vision and retinal pigment epithelial function. EMBO J. 23 (2004), 89–99.
57. [57] Teodoro, J.G., Parker, A.E., Zhu, X., Green, M.R., P53-mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science 313 (2006), 968–971.
58. [58] Paddenberg, R., Faulhammer, P., Goldenberg, A., Kummer, W., Hypoxia-induced increase of endostatin in murine aorta and lung. Histochem. Cell Biol. 125 (2006), 497–508.
59. [59] Wu, P., Yonekura, H., Li, H., Nozaki, I., Tomono, Y., Naito, I., Ninomiya, Y., Yamamoto, H., Hypoxia down-regulates endostatin production by human microvascular endothelial cells and pericytes. Biochem. Biophys. Res. Commun. 288 (2001), 1149–1154.
60. [60] Dhanabal, M., Ramchandran, R., Waterman, M.J., Lu, H., Knebelmann, B., Segal, M., Sukhatme, V.P., Endostatin induces endothelial cell apoptosis. J. Biol. Chem. 274 (1999), 11721–11726.
61. [61] Dixelius, J., Larsson, H., Sasaki, T., Holmqvist, K., Lu, L., Engstrom, A., Timpl, R., Welsh, M., Claesson-Welsh, L., Endostatin-induced tyrosine kinase signaling through the Shb adaptor protein regulates endothelial cell apoptosis. Blood 95 (2000), 3403–3411.
62. [62] Rehn, M., Veikkola, T., Kukk-Valdre, E., Nakamura, H., Ilmonen, M., Lombardo, C., Pihlajaniemi, T., Alitalo, K., Vuori, K., Interaction of endostatin with integrins implicated in angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 1024–1029.
63. [63] Sudhakar, A., Sugimoto, H., Yang, C., Lively, J., Zeisberg, M., Kalluri, R., Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 4766–4771.
64. [64] Wickstrom, S.A., Alitalo, K., Keski-Oja, J., Endostatin associates with integrin alpha5beta1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res. 62 (2002), 5580–5589.
65. [65] Karumanchi, S.A., Jha, V., Ramchandran, R., Karihaloo, A., Tsiokas, L., Chan, B., Dhanabal, M., Hanai, J.I., Venkataraman, G., Shriver, Z., Keiser, N., Kalluri, R., Zeng, H., Mukhopadhyay, D., Chen, R.L., Lander, A.D., Hagihara, K., Yamaguchi, Y., Sasisekharan, R., Cantley, L., Sukhatme, V.P., Cell surface glypicans are low-affinity endostatin receptors. Mol. Cell 7 (2001), 811–822.
66. [66] Wickstrom, S.A., Alitalo, K., Keski-Oja, J., Endostatin associates with lipid rafts and induces reorganization of the actin cytoskeleton via down-regulation of RhoA activity. J. Biol. Chem. 278 (2003), 37895–37901.
67. [67] Kim, Y.M., Hwang, S., Kim, Y.M., Pyun, B.J., Kim, T.Y., Lee, S.T., Gho, Y.S., Kwon, Y.G., Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 277 (2002), 27872–27879.
68. [68] Han, K.Y., Azar, D.T., Sabri, A., Lee, H., Jain, S., Lee, B.S., Chang, J.H., Characterization of the interaction between endostatin short peptide and VEGF receptor 3. Protein Pept. Lett. 19 (2012), 969–974.
69. [69] Han, K.Y., Chang, M., Ying, H.Y., Lee, H., Huang, Y.H., Chang, J.H., Azar, D.T., Selective binding of endostatin peptide 4 to recombinant VEGF receptor 3 in vitro. Protein Pept. Lett. 22 (2015), 1025–1030.
70. [70] Shi, H., Huang, Y., Zhou, H., Song, X., Yuan, S., Fu, Y., Luo, Y., Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood 110 (2007), 2899–2906.
71. [71] Abdollahi, A., Hahnfeldt, P., Maercker, C., Grone, H.J., Debus, J., Ansorge, W., Folkman, J., Hlatky, L., Huber, P.E., Endostatin's antiangiogenic signaling network. Mol. Cell 13 (2004), 649–663.
72. [72] Nyberg, P., Heikkila, P., Sorsa, T., Luostarinen, J., Heljasvaara, R., Stenman, U.H., Pihlajaniemi, T., Salo, T., Endostatin inhibits human tongue carcinoma cell invasion and intravasation and blocks the activation of matrix metalloprotease-2, -9, and -13. J. Biol. Chem. 278 (2003), 22404–22411.
73. [73] Lavergne, E., Hendaoui, I., Coulouarn, C., Ribault, C., Leseur, J., Eliat, P.A., Mebarki, S., Corlu, A., Clement, B., Musso, O., Blocking Wnt signaling by SFRP-like molecules inhibits in vivo cell proliferation and tumor growth in cells carrying active beta-catenin. Oncogene 30 (2011), 423–433.
74. [74] Hendaoui, I., Lavergne, E., Lee, H.S., Hong, S.H., Kim, H.Z., Parent, C., Heuze-Vourc'h, N., Clement, B., Musso, O., Inhibition of Wnt/beta-catenin signaling by a soluble collagen-derived frizzled domain interacting with Wnt3a and the receptors frizzled 1 and 8. PLoS One, 7, 2012, e30601.
75. [75] Tang, Q.Q., Lane, M.D., Adipogenesis: from stem cell to adipocyte. Annu. Rev. Biochem. 81 (2012), 715–736.
76. [76] Iozzo, R.V., Schaefer, L., Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol. 42 (2015), 11–55.
77. [77] Dong, S., Cole, G.J., Halfter, W., Expression of collagen XVIII and localization of its glycosaminoglycan attachment sites. J. Biol. Chem. 278 (2003), 1700–1707.
78. [78] Celie, J.W., Rutjes, N.W., Keuning, E.D., Soininen, R., Heljasvaara, R., Pihlajaniemi, T., Drager, A.M., Zweegman, S., Kessler, F.L., Beelen, R.H., Florquin, S., Aten, J., van den Born, J., Subendothelial heparan sulfate proteoglycans become major L-selectin and monocyte chemoattractant protein-1 ligands upon renal ischemia/reperfusion. Am. J. Pathol. 170 (2007), 1865–1878.
79. [79] Aricescu, A.R., McKinnell, I.W., Halfter, W., Stoker, A.W., Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol. Cell. Biol. 22 (2002), 1881–1892.
80. [80] Hindson, V.J., Gallagher, J.T., Halfter, W., Bishop, P.N., Opticin binds to heparan and chondroitin sulfate proteoglycans. Invest. Ophthalmol. Vis. Sci. 46 (2005), 4417–4423.
81. [81] Balasubramani, M., Schreiber, E.M., Candiello, J., Balasubramani, G.K., Kurtz, J., Halfter, W., Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol. 29 (2010), 471–483.
82. [82] Momota, R., Naito, I., Ninomiya, Y., Ohtsuka, A., Drosophila type XV/XVIII collagen, Mp, is involved in Wingless distribution. Matrix Biol. 30 (2011), 258–266.
83. [83] John, H., Radtke, K., Standker, L., Forssmann, W.G., Identification and characterization of novel endogenous proteolytic forms of the human angiogenesis inhibitors restin and endostatin. Biochim. Biophys. Acta 1747 (2005), 161–170.
84. [84] John, H., Preissner, K.T., Forssmann, W.G., Standker, L., Novel glycosylated forms of human plasma endostatin and circulating endostatin-related fragments of collagen XV. Biochemistry 38 (1999), 10217–10224.
85. [85] Lin, Y., Zhang, S., Rehn, M., Itaranta, P., Tuukkanen, J., Heljasvaara, R., Peltoketo, H., Pihlajaniemi, T., Vainio, S., Induced repatterning of type XVIII collagen expression in ureter bud from kidney to lung type: association with sonic hedgehog and ectopic surfactant protein C. Development 128 (2001), 1573–1585.
86. [86] Carvalhaes, L.S., Gervasio, O.L., Guatimosim, C., Heljasvaara, R., Sormunen, R., Pihlajaniemi, T., Kitten, G.T., Collagen XVIII/endostatin is associated with the epithelial-mesenchymal transformation in the atrioventricular valves during cardiac development. Dev. Dyn. 235 (2006), 132–142.
87. [87] Schuppan, D., Cramer, T., Bauer, M., Strefeld, T., Hahn, E.G., Herbst, H., Hepatocytes as a source of collagen type XVIII endostatin. Lancet 352 (1998), 879–880.
88. [88] Elamaa, H., Sormunen, R., Rehn, M., Soininen, R., Pihlajaniemi, T., Endostatin overexpression specifically in the lens and skin leads to cataract and ultrastructural alterations in basement membranes. Am. J. Pathol. 166 (2005), 221–229.
89. [89] Utriainen, A., Sormunen, R., Kettunen, M., Carvalhaes, L.S., Sajanti, E., Eklund, L., Kauppinen, R., Kitten, G.T., Pihlajaniemi, T., Structurally altered basement membranes and hydrocephalus in a type XVIII collagen deficient mouse line. Hum. Mol. Genet. 13 (2004), 2089–2099.
90. [90] Sasaki, T., Larsson, H., Kreuger, J., Salmivirta, M., Claesson-Welsh, L., Lindahl, U., Hohenester, E., Timpl, R., Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J. 18 (1999), 6240–6248.
91. [91] Ricard-Blum, S., Feraud, O., Lortat-Jacob, H., Rencurosi, A., Fukai, N., Dkhissi, F., Vittet, D., Imberty, A., Olsen, B.R., van der Rest, M., Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling: role of divalent cations. J. Biol. Chem. 279 (2004), 2927–2936.
92. [92] Sasaki, T., Larsson, H., Tisi, D., Claesson-Welsh, L., Hohenester, E., Timpl, R., Endostatins derived from collagens XV and XVIII differ in structural and binding properties, tissue distribution and anti-angiogenic activity. J. Mol. Biol. 301 (2000), 1179–1190.
93. [93] Javaherian, K., Park, S.Y., Pickl, W.F., LaMontagne, K.R., Sjin, R.T., Gillies, S., Lo, K.M., Laminin modulates morphogenic properties of the collagen XVIII endostatin domain. J. Biol. Chem. 277 (2002), 45211–45218.
94. [94] Faye, C., Chautard, E., Olsen, B.R., Ricard-Blum, S., The first draft of the endostatin interaction network. J. Biol. Chem. 284 (2009), 22041–22047.
95. [95] Marneros, A.G., Olsen, B.R., Physiological role of collagen XVIII and endostatin. FASEB J. 19 (2005), 716–728.
96. [96] Fukai, N., Eklund, L., Marneros, A.G., Oh, S.P., Keene, D.R., Tamarkin, L., Niemela, M., Ilves, M., Li, E., Pihlajaniemi, T., Olsen, B.R., Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J. 21 (2002), 1535–1544.
97. [97] Ylikarppa, R., Eklund, L., Sormunen, R., Kontiola, A.I., Utriainen, A., Maatta, M., Fukai, N., Olsen, B.R., Pihlajaniemi, T., Lack of type XVIII collagen results in anterior ocular defects. FASEB J. 17 (2003), 2257–2259.
98. [98] Rygh, C.B., Lokka, G., Heljasvaara, R., Taxt, T., Pavlin, T., Sormunen, R., Pihlajaniemi, T., Curry, F.R., Tenstad, O., Reed, R.K., Image-based assessment of microvascular function and structure in collagen XV- and XVIII-deficient mice. J. Physiol. 592 (2014), 325–336.
99. [99] Khan, A.O., Aldahmesh, M.A., Mohamed, J.Y., Al-Mesfer, S., Alkuraya, F.S., The distinct ophthalmic phenotype of Knobloch syndrome in children. Br. J. Ophthalmol. 96 (2012), 890–895.
100. [100] Sertie, A.L., Quimby, M., Moreira, E.S., Murray, J., Zatz, M., Antonarakis, S.E., Passos-Bueno, M.R., A gene which causes severe ocular alterations and occipital encephalocele (Knobloch syndrome) is mapped to 21q22.3. Hum. Mol. Genet. 5 (1996), 843–847.
101. [101] Sertie, A.L., Sossi, V., Camargo, A.A., Zatz, M., Brahe, C., Passos-Bueno, M.R., Collagen XVIII, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum. Mol. Genet. 9 (2000), 2051–2058.
102. [102] Bishop, J.R., Passos-Bueno, M.R., Fong, L., Stanford, K.I., Gonzales, J.C., Yeh, E., Young, S.G., Bensadoun, A., Witztum, J.L., Esko, J.D., Moulton, K.S., Deletion of the basement membrane heparan sulfate proteoglycan type XVIII collagen causes hypertriglyceridemia in mice and humans. PLoS One, 5, 2010, e13919.
103. [103] Czeizel, A.E., Goblyos, P., Kustos, G., Mester, E., Paraicz, E., The second report of Knobloch syndrome. Am. J. Med. Genet. 42 (1992), 777–779.
104. [104] Duh, E.J., Yao, Y.G., Dagli, M., Goldberg, M.F., Persistence of fetal vasculature in a patient with Knobloch syndrome: potential role for endostatin in fetal vascular remodeling of the eye. Ophthalmology 111 (2004), 1885–1888.
105. [105] Kliemann, S.E., Waetge, R.T., Suzuki, O.T., Passos-Bueno, M.R., Rosemberg, S., Evidence of neuronal migration disorders in Knobloch syndrome: clinical and molecular analysis of two novel families. Am. J. Med. Genet. A 119A (2003), 15–19.
106. [106] Mahajan, V.B., Olney, A.H., Garrett, P., Chary, A., Dragan, E., Lerner, G., Murray, J., Bassuk, A.G., Collagen XVIII mutation in Knobloch syndrome with acute lymphoblastic leukemia. Am. J. Med. Genet. A 152A (2010), 2875–2879.
107. [107] Williams, T.A., Kirkby, G.R., Williams, D., Ainsworth, J.R., A phenotypic variant of Knobloch syndrome. Ophthalmic Genet. 29 (2008), 85–86.
108. [108] Maatta, M., Heljasvaara, R., Pihlajaniemi, T., Uusitalo, M., Collagen XVIII/endostatin shows a ubiquitous distribution in human ocular tissues and endostatin-containing fragments accumulate in ocular fluid samples. Graefes Arch. Clin. Exp. Ophthalmol. 245 (2007), 74–81.
109. [109] Uechi, G., Sun, Z., Schreiber, E.M., Halfter, W., Balasubramani, M., Proteomic view of basement membranes from human retinal blood vessels, inner limiting membranes, and lens capsules. J. Proteome Res., 2014.
110. [110] Hurskainen, M., Eklund, L., Hagg, P.O., Fruttiger, M., Sormunen, R., Ilves, M., Pihlajaniemi, T., Abnormal maturation of the retinal vasculature in type XVIII collagen/endostatin deficient mice and changes in retinal glial cells due to lack of collagen types XV and XVIII. FASEB J. 19 (2005), 1564–1566.
111. [111] Marneros, A.G., Olsen, B.R., Age-dependent iris abnormalities in collagen XVIII/endostatin deficient mice with similarities to human pigment dispersion syndrome. Invest. Ophthalmol. Vis. Sci. 44 (2003), 2367–2372.
112. [112] Ylikarppa, R., Eklund, L., Sormunen, R., Muona, A., Fukai, N., Olsen, B.R., Pihlajaniemi, T., Double knockout mice reveal a lack of major functional compensation between collagens XV and XVIII. Matrix Biol. 22 (2003), 443–448.
113. [113] Seaver, L.H., Joffe, L., Spark, R.P., Smith, B.L., Hoyme, H.E., Congenital scalp defects and vitreoretinal degeneration: redefining the Knobloch syndrome. Am. J. Med. Genet. 46 (1993), 203–208.
114. [114] Passos-Bueno, M.R., Marie, S.K., Monteiro, M., Neustein, I., Whittle, M.R., Vainzof, M., Zatz, M., Knobloch syndrome in a large Brazilian consanguineous family: confirmation of autosomal recessive inheritance. Am. J. Med. Genet. 52 (1994), 170–173.
115. [115] Kivinen, N., Felszeghy, S., Kinnunen, A.I., Setala, N., Aikio, M., Kinnunen, K., Sironen, R., Pihlajaniemi, T., Kauppinen, A., Kaarniranta, K., Absence of collagen XVIII in mice causes age-related insufficiency in retinal pigment epithelium proteostasis. Biogerontology, 2016.
116. [116] Rossi, M., Morita, H., Sormunen, R., Airenne, S., Kreivi, M., Wang, L., Fukai, N., Olsen, B.R., Tryggvason, K., Soininen, R., Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 22 (2003), 236–245.
117. [117] Campbell, M., Collery, R., McEvoy, A., Gardiner, T.A., Stitt, A.W., Brankin, B., Involvement of MAPKs in endostatin-mediated regulation of blood-retinal barrier function. Curr. Eye Res. 31 (2006), 1033–1045.
118. [118] Mori, K., Ando, A., Gehlbach, P., Nesbitt, D., Takahashi, K., Goldsteen, D., Penn, M., Chen, C.T., Mori, K., Melia, M., Phipps, S., Moffat, D., Brazzell, K., Liau, G., Dixon, K.H., Campochiaro, P.A., Inhibition of choroidal neovascularization by intravenous injection of adenoviral vectors expressing secretable endostatin. Am. J. Pathol. 159 (2001), 313–320.
119. [119] Takahashi, K., Saishin, Y., Saishin, Y., Silva, R.L., Oshima, Y., Oshima, S., Melia, M., Paszkiet, B., Zerby, D., Kadan, M.J., Liau, G., Kaleko, M., Connelly, S., Luo, T., Campochiaro, P.A., Intraocular expression of endostatin reduces VEGF-induced retinal vascular permeability, neovascularization, and retinal detachment. FASEB J. 17 (2003), 896–898.
120. [120] Schneider, V.A., Granato, M., The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50 (2006), 683–695.
121. [121] Banerjee, S., Isaacman-Beck, J., Schneider, V.A., Granato, M., A novel role for Lh3 dependent ECM modifications during neural crest cell migration in zebrafish. PLoS One, 8, 2013, e54609.
122. [122] Zhang, J., Williams, M.A., Rigamonti, D., Genetics of human hydrocephalus. J. Neurol. 253 (2006), 1255–1266.
123. [123] Morawski, M., Filippov, M., Tzinia, A., Tsilibary, E., Vargova, L., ECM in brain aging and dementia. Prog. Brain Res. 214 (2014), 207–227.
124. [124] Ancsin, J.B., Amyloidogenesis: historical and modern observations point to heparan sulfate proteoglycans as a major culprit. Amyloid 10 (2003), 67–79.
125. [125] Cui, H., Freeman, C., Jacobson, G.A., Small, D.H., Proteoglycans in the central nervous system: role in development, neural repair, and Alzheimer's disease. IUBMB Life 65 (2013), 108–120.
126. [126] Hosono-Fukao, T., Ohtake-Niimi, S., Hoshino, H., Britschgi, M., Akatsu, H., Hossain, M.M., Nishitsuji, K., van Kuppevelt, T.H., Kimata, K., Michikawa, M., Wyss-Coray, T., Uchimura, K., Heparan sulfate subdomains that are degraded by Sulf accumulate in cerebral amyloid ss plaques of Alzheimer's disease: evidence from mouse models and patients. Am. J. Pathol. 180 (2012), 2056–2067.
127. [127] van Horssen, J., Wilhelmus, M.M., Heljasvaara, R., Pihlajaniemi, T., Wesseling, P., de Waal, R.M., Verbeek, M.M., Collagen XVIII: a novel heparan sulfate proteoglycan associated with vascular amyloid depositions and senile plaques in Alzheimer's disease brains. Brain Pathol. 12 (2002), 456–462.
128. [128] Deininger, M.H., Fimmen, B.A., Thal, D.R., Schluesener, H.J., Meyermann, R., Aberrant neuronal and paracellular deposition of endostatin in brains of patients with Alzheimer's disease. J. Neurosci. 22 (2002), 10621–10626.
129. [129] Kranenburg, O., Kroon-Batenburg, L.M., Reijerkerk, A., Wu, Y.P., Voest, E.E., Gebbink, M.F., Recombinant endostatin forms amyloid fibrils that bind and are cytotoxic to murine neuroblastoma cells in vitro. FEBS Lett. 539 (2003), 149–155.
130. [130] Zhao, H., Jutila, A., Nurminen, T., Wickstrom, S.A., Keski-Oja, J., Kinnunen, P.K., Binding of endostatin to phosphatidylserine-containing membranes and formation of amyloid-like fibers. Biochemistry 44 (2005), 2857–2863.
131. [131] He, Y., Zhou, H., Tang, H., Luo, Y., Deficiency of disulfide bonds facilitating fibrillogenesis of endostatin. J. Biol. Chem. 281 (2006), 1048–1057.
132. [132] Salza, R., Oudart, J.B., Ramont, L., Maquart, F.X., Bakchine, S., Thoannes, H., Ricard-Blum, S., Endostatin level in cerebrospinal fluid of patients with Alzheimer's disease. J. Alzheimers Dis. 44 (2015), 1253–1261.
133. [133] Wiseman, F.K., Al-Janabi, T., Hardy, J., Karmiloff-Smith, A., Nizetic, D., Tybulewicz, V.L., Fisher, E.M., Strydom, A., A genetic cause of Alzheimer disease: mechanistic insights from Down syndrome. Nat. Rev. Neurosci. 16 (2015), 564–574.
134. [134] Liu, C.C., Kanekiyo, T., Xu, H., Bu, G., Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 9 (2013), 106–118.
135. [135] Ackley, B.D., Kang, S.H., Crew, J.R., Suh, C., Jin, Y., Kramer, J.M., The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J. Neurosci. 23 (2003), 3577–3587.
136. [136] Kuo, C.J., LaMontagne, K.R. Jr., Garcia-Cardena, G., Ackley, B.D., Kalman, D., Park, S., Christofferson, R., Kamihara, J., Ding, Y.H., Lo, K.M., Gillies, S., Folkman, J., Mulligan, R.C., Javaherian, K., Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain. J. Cell Biol. 152 (2001), 1233–1246.
137. [137] Meyer, F., Moussian, B., Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Develop. Growth Differ. 51 (2009), 483–498.
138. [138] Hamano, Y., Okude, T., Shirai, R., Sato, I., Kimura, R., Ogawa, M., Ueda, Y., Yokosuka, O., Kalluri, R., Ueda, S., Lack of collagen XVIII/endostatin exacerbates immune-mediated glomerulonephritis. J. Am. Soc. Nephrol. 21 (2010), 1445–1455.
139. [139] Karihaloo, A., Karumanchi, S.A., Barasch, J., Jha, V., Nickel, C.H., Yang, J., Grisaru, S., Bush, K.T., Nigam, S., Rosenblum, N.D., Sukhatme, V.P., Cantley, L.G., Endostatin regulates branching morphogenesis of renal epithelial cells and ureteric bud. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 12509–12514.
140. [140] Charytan, D.M., Padera, R., Helfand, A.M., Zeisberg, M., Xu, X., Liu, X., Himmelfarb, J., Cinelli, A., Kalluri, R., Zeisberg, E.M., Increased concentration of circulating angiogenesis and nitric oxide inhibitors induces endothelial to mesenchymal transition and myocardial fibrosis in patients with chronic kidney disease. Int. J. Cardiol. 176 (2014), 99–109.
141. [141] Chen, J., Hamm, L.L., Mohler, E.R., Hudaihed, A., Arora, R., Chen, C.S., Liu, Y., Browne, G., Mills, K.T., Kleinpeter, M.A., Simon, E.E., Rifai, N., Klag, M.J., He, J., Interrelationship of multiple endothelial dysfunction biomarkers with chronic kidney disease. PLoS One, 10, 2015, e0132047.
142. [142] Ruge, T., Carlsson, A.C., Larsson, T.E., Carrero, J.J., Larsson, A., Lind, L., Arnlov, J., Endostatin level is associated with kidney injury in the elderly: findings from two community-based cohorts. Am. J. Nephrol. 40 (2014), 417–424.
143. [143] Rydzewska-Rosolowska, A., Borawski, J., Mysliwiec, M., High plasma endostatin level unaffected by low-molecular weight heparin in hemodialysis patients—a preliminary report. Adv. Med. Sci. 54 (2009), 199–202.
144. [144] Stoessel, A., Paliege, A., Theilig, F., Addabbo, F., Ratliff, B., Waschke, J., Patschan, D., Goligorsky, M.S., Bachmann, S., Indolent course of tubulointerstitial disease in a mouse model of subpressor, low-dose nitric oxide synthase inhibition. Am. J. Physiol. Ren. Physiol. 295 (2008), F717–F725.
145. [145] Maciel, T.T., Coutinho, E.L., Soares, D., Achar, E., Schor, N., Bellini, M.H., Endostatin, an antiangiogenic protein, is expressed in the unilateral ureteral obstruction mice model. J. Nephrol. 21 (2008), 753–760.
146. [146] Pushpakumar, S.B., Kundu, S., Metreveli, N., Sen, U., Folic acid mitigates angiotensin-II-induced blood pressure and renal remodeling. PLoS One, 8, 2013, e83813.
147. [147] Carlsson, A.C., Ruge, T., Sundstrom, J., Ingelsson, E., Larsson, A., Lind, L., Arnlov, J., Association between circulating endostatin, hypertension duration, and hypertensive target-organ damage. Hypertension 62 (2013), 1146–1151.
148. [148] Carlsson, A.C., Ostgren, C.J., Lanne, T., Larsson, A., Nystrom, F.H., Arnlov, J., The association between endostatin and kidney disease and mortality in patients with type 2 diabetes. Diabete Metab., 2016.
149. [149] Musso, O., Theret, N., Heljasvaara, R., Rehn, M., Turlin, B., Campion, J.P., Pihlajaniemi, T., Clement, B., Tumor hepatocytes and basement membrane-producing cells specifically express two different forms of the endostatin precursor, collagen XVIII, in human liver cancers. Hepatology 33 (2001), 868–876.
150. [150] Jia, J.D., Bauer, M., Sedlaczek, N., Herbst, H., Ruehl, M., Hahn, E.G., Riecken, E.O., Schuppan, D., Modulation of collagen XVIII/endostatin expression in lobular and biliary rat liver fibrogenesis. J. Hepatol. 35 (2001), 386–391.
151. [151] Duncan, M.B., Yang, C., Tanjore, H., Boyle, P.M., Keskin, D., Sugimoto, H., Zeisberg, M., Olsen, B.R., Kalluri, R., Type XVIII collagen is essential for survival during acute liver injury in mice. Dis. Model. Mech. 6 (2013), 942–951.
152. [152] Musso, O., Rehn, M., Theret, N., Turlin, B., Bioulac-Sage, P., Lotrian, D., Campion, J.P., Pihlajaniemi, T., Clement, B., Tumor progression is associated with a significant decrease in the expression of the endostatin precursor collagen XVIII in human hepatocellular carcinomas. Cancer Res. 61 (2001), 45–49.
153. [153] Dhar, D.K., Ono, T., Yamanoi, A., Soda, Y., Yamaguchi, E., Rahman, M.A., Kohno, H., Nagasue, N., Serum endostatin predicts tumor vascularity in hepatocellular carcinoma. Cancer 95 (2002), 2188–2195.
154. [154] Hu, T.H., Huang, C.C., Wu, C.L., Lin, P.R., Liu, S.Y., Lin, J.W., Chuang, J.H., Tai, M.H., Increased endostatin/collagen XVIII expression correlates with elevated VEGF level and poor prognosis in hepatocellular carcinoma. Mod. Pathol. 18 (2005), 663–672.
155. [155] Lietard, J., Theret, N., Rehn, M., Musso, O., Dargere, D., Pihlajaniemi, T., Clement, B., The promoter of the long variant of collagen XVIII, the precursor of endostatin, contains liver-specific regulatory elements. Hepatology 32 (2000), 1377–1385.
156. [156] Inoue-Murayama, M., Sugimoto, Y., Niimi, Y., Aso, H., Type XVIII collagen is newly transcribed during bovine adipogenesis. Differentiation 65 (2000), 281–285.
157. [157] Errera, F.I., Canani, L.H., Yeh, E., Kague, E., Armelin-Correa, L.M., Suzuki, O.T., Tschiedel, B., Silva, M.E., Sertie, A.L., Passos-Bueno, M.R., COL18A1 is highly expressed during human adipocyte differentiation and the SNP c.1136C > T in its “frizzled” motif is associated with obesity in diabetes type 2 patients. An. Acad. Bras. Cienc. 80 (2008), 167–177.
158. [158] Ross, S.E., Hemati, N., Longo, K.A., Bennett, C.N., Lucas, P.C., Erickson, R.L., MacDougald, O.A., Inhibition of adipogenesis by Wnt signaling. Science 289 (2000), 950–953.
159. [159] Bowers, R.R., Lane, M.D., Wnt signaling and adipocyte lineage commitment. Cell Cycle 7 (2008), 1191–1196.
160. [160] North, K.E., Miller, M.B., Coon, H., Martin, L.J., Peacock, J.M., Arnett, D., Zhang, B., Province, M., Oberman, A., Blangero, J., Almasy, L., Ellison, R.C., Heiss, G., Evidence for a gene influencing fasting LDL cholesterol and triglyceride levels on chromosome 21q. Atherosclerosis 179 (2005), 119–125.
161. [161] Peloso, G.M., Auer, P.L., Bis, J.C., Voorman, A., Morrison, A.C., Brody, J.A., Khetarpal, S.A., Crosby, J.R., Fornage, M., Isaacs, A., Jakobsdottir, J., Feitosa, M.F., Davies, G., Huffman, J.E., Manichaikul, A., Davis, B., Lohman, K., Joon, A.Y., Smith, A.V., Grove, M.L., Zanoni, P., Redon, V., Demissie, S., Lawson, K., Peters, U., Carlson, C., Jackson, R.D., Ryckman, K.K., Mackey, R.H., Robinson, J.G., Siscovick, D.S., Schreiner, P.J., Mychaleckyj, J.C., Pankow, J.S., Hofman, A., Uitterlinden, A.G., Harris, T.B., Taylor, K.D., Stafford, J.M., Reynolds, L.M., Marioni, R.E., Dehghan, A., Franco, O.H., Patel, A.P., Lu, Y., Hindy, G., Gottesman, O., Bottinger, E.P., Melander, O., Orho-Melander, M., Loos, R.J., Duga, S., Merlini, P.A., Farrall, M., Goel, A., Asselta, R., Girelli, D., Martinelli, N., Shah, S.H., Kraus, W.E., Li, M., Rader, D.J., Reilly, M.P., McPherson, R., Watkins, H., Ardissino, D., NHLBI GO Exome Sequencing Project, Zhang, Q., Wang, J., Tsai, M.Y., Taylor, H.A., Correa, A., Griswold, M.E., Lange, L.A., Starr, J.M., Rudan, I., Eiriksdottir, G., Launer, L.J., Ordovas, J.M., Levy, D., Chen, Y.D., Reiner, A.P., Hayward, C., Polasek, O., Deary, I.J., Borecki, I.B., Liu, Y., Gudnason, V., Wilson, J.G., van Duijn, C.M., Kooperberg, C., Rich, S.S., Psaty, B.M., Rotter, J.I., O'Donnell, C.J., Rice, K., Boerwinkle, E., Kathiresan, S., Cupples, L.A., Association of low-frequency and rare coding-sequence variants with blood lipids and coronary heart disease in 56,000 whites and blacks. Am. J. Hum. Genet. 94 (2014), 223–232.
162. [162] Bao, Y., Peng, F., Zhou, Q.C., Yu, Z.H., Li, J.C., Cheng, Z.B., Chen, L., Hu, X., Chen, Y.Y., Wang, J., Wang, Y., Ma, H.L., Xu, Z.M., Lu, R.B., Deng, X.W., Chen, M., Phase II trial of recombinant human endostatin in combination with concurrent chemoradiotherapy in patients with stage III non-small-cell lung cancer. Radiother. Oncol. 114 (2015), 161–166.
163. [163] Jiang, X., Guan, W., Li, M., Liang, W., Qing, Y., Dai, N., Zhang, S., Deng, Y., Meng, H., Yang, Y., Zhong, Z., Endostatin combined with platinum-based chemo-radiotherapy for advanced non-small cell lung cancer. Cell Biochem. Biophys. 71 (2015), 571–577.
164. [164] Chen, J., Yao, Q., Li, D., Zhang, J., Wang, T., Yu, M., Zhou, X., Huan, Y., Wang, J., Wang, L., Neoadjuvant rh-endostatin, docetaxel and epirubicin for breast cancer: efficacy and safety in a prospective, randomized, phase II study. BMC Cancer, 13, 2013 (248-2407-13-248).
165. [165] Cui, C., Mao, L., Chi, Z., Si, L., Sheng, X., Kong, Y., Li, S., Lian, B., Gu, K., Tao, M., Song, X., Lin, T., Ren, X., Qin, S., Guo, J., A phase II, randomized, double-blind, placebo-controlled multicenter trial of Endostar in patients with metastatic melanoma. Mol. Ther. 21 (2013), 1456–1463.
166. [166] Ye, W., Liu, R., Pan, C., Jiang, W., Zhang, L., Guan, Z., Wu, J., Ying, X., Li, L., Li, S., Tan, W., Zeng, M., Kang, T., Liu, Q., Thomas, G.R., Huang, M., Deng, W., Huang, W., Multicenter randomized phase 2 clinical trial of a recombinant human endostatin adenovirus in patients with advanced head and neck carcinoma. Mol. Ther. 22 (2014), 1221–1229.
167. [167] Sun, X.J., Deng, Q.H., Yu, X.M., Ji, Y.L., Zheng, Y.D., Jiang, H., Xu, Y.P., Ma, S.L., A phase II study of Endostatin in combination with paclitaxel, carboplatin, and radiotherapy in patients with unresectable locally advanced non-small cell lung cancer. BMC Cancer, 16, 2016 (266-016-2234-0).
168. [168] Lu, S., Li, L., Luo, Y., Zhang, L., Wu, G., Chen, Z., Huang, C., Guo, S., Zhang, Y., Song, X., Yu, Y., Zhou, C., Li, W., Liao, M., Li, B., Xu, L., Chen, P., Hu, C., Hu, C., A multicenter, open-label, randomized phase II controlled study of rh-endostatin (Endostar) in combination with chemotherapy in previously untreated extensive-stage small-cell lung cancer. J. Thorac. Oncol. 10 (2015), 206–211.
169. [169] Karppinen, S.M., Honkanen, H.K., Heljasvaara, R., Riihila, P., Autio-Harmainen, H., Sormunen, R., Harjunen, V., Vaisanen, M.R., Vaisanen, T., Hurskainen, T., Tasanen, K., Kahari, V.M., Pihlajaniemi, T., Collagens XV and XVIII show different expression and localisation in cutaneous squamous cell carcinoma: type XV appears in tumor stroma, while XVIII becomes upregulated in tumor cells and lost from microvessels. Exp. Dermatol. 25 (2016), 348–354.
170. [170] Vaananen, A., Ylipalosaari, M., Parikka, M., Kainulainen, T., Rehn, M., Heljasvaara, R., Tjaderhane, L., Salo, T., Collagen XVIII modulation is altered during progression of oral dysplasia and carcinoma. J. Oral Pathol. Med. 36 (2007), 35–42.
171. [171] Iizasa, T., Chang, H., Suzuki, M., Otsuji, M., Yokoi, S., Chiyo, M., Motohashi, S., Yasufuku, K., Sekine, Y., Iyoda, A., Shibuya, K., Hiroshima, K., Fujisawa, T., Overexpression of collagen XVIII is associated with poor outcome and elevated levels of circulating serum endostatin in non-small cell lung cancer. Clin. Cancer Res. 10 (2004), 5361–5366.
172. [172] Balasubramanian, S.P., Cross, S.S., Globe, J., Cox, A., Brown, N.J., Reed, M.W., Endostatin gene variation and protein levels in breast cancer susceptibility and severity. BMC Cancer, 7, 2007, 107.
173. [173] Ohlund, D., Ardnor, B., Oman, M., Naredi, P., Sund, M., Expression pattern and circulating levels of endostatin in patients with pancreas cancer. Int. J. Cancer 122 (2008), 2805–2810.
174. [174] Guenther, U., Herbst, H., Bauer, M., Isbert, C., Buhr, H.J., Riecken, E.O., Schuppan, D., Collagen type XVIII/endostatin is differentially expressed in primary and metastatic colorectal cancers and ovarian carcinomas. Br. J. Cancer 85 (2001), 1540–1545.
175. [175] Maatta, M., Butzow, R., Luostarinen, J., Petajaniemi, N., Pihlajaniemi, T., Salo, S., Miyazaki, K., Autio-Harmainen, H., Virtanen, I., Differential expression of laminin isoforms in ovarian epithelial carcinomas suggesting different origin and providing tools for differential diagnosis. J. Histochem. Cytochem. 53 (2005), 1293–1300.
176. [176] Aref, S., El-Sherbiny, M., Azmy, E., Goda, T., Selim, T., El-Refaie, M., Twafik, E., Elevated serum endostatin levels are associated with favorable outcome in acute myeloid leukemia. Hematology 13 (2008), 95–100.
177. [177] Slater, A.A., Alokail, M., Gentle, D., Yao, M., Kovacs, G., Maher, E.R., Latif, F., DNA methylation profiling distinguishes histological subtypes of renal cell carcinoma. Epigenetics 8 (2013), 252–267.
178. [178] Chernov, A.V., Baranovskaya, S., Golubkov, V.S., Wakeman, D.R., Snyder, E.Y., Williams, R., Strongin, A.Y., Microarray-based transcriptional and epigenetic profiling of matrix metalloproteinases, collagens, and related genes in cancer. J. Biol. Chem. 285 (2010), 19647–19659.
179. [179] Brideau, G., Makinen, M.J., Elamaa, H., Tu, H., Nilsson, G., Alitalo, K., Pihlajaniemi, T., Heljasvaara, R., Endostatin overexpression inhibits lymphangiogenesis and lymph node metastasis in mice. Cancer Res. 67 (2007), 11528–11535.
180. [180] Sund, M., Hamano, Y., Sugimoto, H., Sudhakar, A., Soubasakos, M., Yerramalla, U., Benjamin, L.E., Lawler, J., Kieran, M., Shah, A., Kalluri, R., Function of endogenous inhibitors of angiogenesis as endothelium-specific tumor suppressors. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 2934–2939.
181. [181] Hasle, H., Clemmensen, I.H., Mikkelsen, M., Risks of leukaemia and solid tumours in individuals with Down's syndrome. Lancet 355 (2000), 165–169.
182. [182] Hasle, H., Friedman, J.M., Olsen, J.H., Rasmussen, S.A., Low risk of solid tumors in persons with Down syndrome. Genitourin. Med., 2016.
183. [183] Ivanova, N.B., Dimos, J.T., Schaniel, C., Hackney, J.A., Moore, K.A., Lemischka, I.R., A stem cell molecular signature. Science 298 (2002), 601–604.
184. [184] Blanpain, C., Lowry, W.E., Geoghegan, A., Polak, L., Fuchs, E., Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118 (2004), 635–648.
185. [185] Gupta, P.B., Onder, T.T., Jiang, G., Tao, K., Kuperwasser, C., Weinberg, R.A., Lander, E.S., Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138 (2009), 645–659.