Cathepsin G-Induced Insulin-Like Growth Factor (IGF) Elevation in MCF-7 Medium Is Caused by Proteolysis of IGF Binding Protein (IGFBP)-2 but Not of IGF-1

1) Yuan Y, Jiang YC, Sun CK, Chen QM. Role of the tumor microenvironment in tumor progression and the clinical applications. <i>Oncol. Rep.</i>, <b>35</b>, 2499–2515 (2016).

2) Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. <i>J. Cell Sci.</i>, <b>125</b>, 5591–5596 (2012).

3) Powell DR, Huttenlocher A. Neutrophils in the tumor microenvironment. <i>Trends Immunol.</i>, <b>37</b>, 41–52 (2016).

4) Kim J, Bae JS. Tumor-associated macrophages and neutrophils in tumor microenvironment. <i>Mediators Inflamm.</i>, <b>2016</b>, 6058147 (2016).

5) Shaul ME, Fridlender ZG. Cancer-related circulating and tumor-associated neutrophils—subtypes, sources and function. <i>FEBS J.</i>, <b>285</b>, 4316–4342 (2018).

6) Yui S, Tomita K, Kudo T, Ando S, Yamazaki M. Induction of multicellular 3-D spheroids of MCF-7 breast carcinoma cells by neutrophil-derived cathepsin G and elastase. <i>Cancer Sci.</i>, <b>96</b>, 560–570 (2005).

7) Kudo T, Kigoshi H, Hagiwara T, Takino T, Yamazaki M, Yui S. Cathepsin G, a neutrophil protease, induces compact cell-cell adhesion in MCF-7 human breast cancer cells. <i>Mediators Inflamm.</i>, <b>2009</b>, 850940 (2009).

8) Morimoto-Kamata R, Mizoguchi S, Ichisugi T, Yui S. Cathepsin G induces cell aggregation of human breast cancer MCF-7 cells <i>via</i> a 2-step mechanism: catalytic site-independent binding to the cell surface and enzymatic activity-dependent induction of the cell aggregation. <i>Mediators Inflamm.</i>, <b>2012</b>, 456462 (2012).

9) Morimoto-Kamata R, Yui S. Insulin-like growth factor-1 signaling is responsible for cathepsin G-induced aggregation of breast cancer MCF-7 cells. <i>Cancer Sci.</i>, <b>108</b>, 1574–1583 (2017).

10) Pollak M. Insulin and insulin-like growth factor signaling in neoplasia. <i>Nat. Rev. Cancer</i>, <b>8</b>, 915–928 (2008).

11) Brahmkhatri VP, Prasanna C, Atreya HS. Insulin-like growth factor system in cancer: novel targeted therapies. <i>Biomed. Res. Int.</i>, <b>2015</b>, 538019 (2015).

12) Christopoulos PF, Msaouel P, Koutsilieris M. The role of the insulin-like growth factor-1 system in breast cancer. <i>Mol. Cancer</i>, <b>14</b>, 43 (2015).

13) Allard JB, Duan C. IGF-binding proteins: why do they exist and why are there so many? <i>Front. Endocrinol.</i> (Lausanne), <b>9</b>, 117 (2018).

14) Peyrat JP, Bonneterre J, Vennin PH, Jammes H, Beuscart R, Hecquet B, Djiane J, Lefebvre J, Demaille A. Insulin-like growth factor 1 receptors (IGF1-R) and IGF1 in human breast tumors. <i>J. Steroid Biochem. Mol. Biol.</i>, <b>37</b>, 823–827 (1990).

15) Firth SM, Baxter RC. Cellular actions of the insulin-like growth factor binding proteins. <i>Endocr. Rev.</i>, <b>23</b>, 824–854 (2002).

16) Mark S, Kübler B, Höning S, Oesterreicher S, John H, Braulke T, Forssmann WG, Ständker L. Diversity of human insulin-like growth factor (IGF) binding protein-2 fragments in plasma: primary structure, IGF-binding properties, and disulfide bonding pattern. <i>Biochemistry</i>, <b>44</b>, 3644–3652 (2005).

17) Kibbey MM, Jameson MJ, Eaton EM, Rosenzweig SA. Insulin-like growth factor binding protein-2: contributions of the C-terminal domain to insulin-like growth factor-1 binding. <i>Mol. Pharmacol.</i>, <b>69</b>, 833–845 (2006).

18) Kuang Z, Yao S, McNeil KA, Thompson JA, Bach LA, Forbes BE, Wallace JC, Norton RS. Cooperativity of the N- and C-terminal domains of insulin-like growth factor (IGF) binding protein 2 in IGF binding. <i>Biochemistry</i>, <b>46</b>, 13720–13732 (2007).

19) Rajah R, Katz L, Nunn S, Solberg P, Beers T, Cohen P. Insulin-like growth factor binding protein (IGFBP) proteases: functional regulators of cell growth. <i>Prog. Growth Factor Res.</i>, <b>6</b>, 273–284 (1995).

20) Bunn RC, Fowlkes JL. Insulin-like growth factor binding protein proteolysis. <i>Trends Endocrinol. Metab.</i>, <b>14</b>, 176–181 (2003).

21) Gibson TL, Cohen P. Inflammation-related neutrophil proteases, cathepsin G and elastase, function as insulin-like growth factor binding protein proteases. <i>Growth Horm. IGF Res.</i>, <b>9</b>, 241–253 (1999).

22) Yui S, Osawa Y, Ichisugi T, Morimoto-Kamata R. Neutrophil cathepsin G, but not elastase, induces aggregation of MCF-7 mammary carcinoma cells by a protease activity-dependent cell-oriented mechanism. <i>Mediators Inflamm.</i>, <b>2014</b>, 971409 (2014).

23) McGuire WL Jr, Jackson JG, Figueroa JA, Shimasaki S, Powell DR, Yee D. Regulation of insulin-like growth factor-binding protein (IGFBP) expression by breast cancer cells: use of IGFBP-1 as an inhibitor of insulin-like growth factor action. <i>J. Natl. Cancer Inst.</i>, <b>84</b>, 1336–1341 (1992).

24) Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR, Jenkins KM, Beaulieu KA, Mouded M, Frank SJ, Wong KK, Shapiro SD. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. <i>Nat. Med.</i>, <b>16</b>, 219–223 (2010).

25) Gregory AD, Hale P, Perlmutter DH, Houghton AM. Clathrin pit-mediated endocytosis of neutrophil elastase and cathepsin G by cancer cells. <i>J. Biol. Chem.</i>, <b>287</b>, 35341–35350 (2012).

26) Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. <i>Cell</i>, <b>141</b>, 1117–1134 (2010).

27) Kavran JM, McCabe JM, Byrne PO, Connacher MK, Wang Z, Ramek A, Sarabipour S, Shan Y, Shaw DE, Hristova K, Cole PA, Leahy DJ. How IGF-1 activates its receptor. <i>eLife</i>, <b>3</b>, e03772 (2014).

28) Frattali AL, Treadway JL, Pessin JE. Transmembrane signaling by the human insulin receptor kinase. Relationship between intramolecular β subunit <i>trans</i>- and <i>cis</i>-autophosphorylation and substrate kinase activation. <i>J. Biol. Chem.</i>, <b>267</b>, 19521–19528 (1992).

29) Leef JW, Larner J. Insulin-mimetic effect of trypsin on the insulin receptor tyrosine kinase in intact adipocytes. <i>J. Biol. Chem.</i>, <b>262</b>, 14837–14842 (1987).

30) Nakajima K, Powers JC, Ashe BM, Zimmerman M. Mapping the extended substrate binding site of cathepsin G and human leukocyte elastase. Studies with peptide substrates related to the α1-protease inhibitor reactive site. <i>J. Biol. Chem.</i>, <b>254</b>, 4027–4032 (1979).

31) McRae B, Nakajima K, Travis J, Powers JC. Studies on reactivity of human leukocyte elastase, cathepsin G, and porcine pancreatic elastase toward peptides including sequences related to the reactive site of α1-protease inhibitor (α1-antitrypsin). <i>Biochemistry</i>, <b>19</b>, 3973–3978 (1980).

32) Tanaka T, Minematsu Y, Reilly CF, Travis J, Powers JC. Human leukocyte cathepsin G. Subsite mapping with 4-nitroanilides, chemical modification and effect of possible cofactors. <i>Biochemistry</i>, <b>24</b>, 2040–2047 (1985).

33) Réhault S, Brillard-Bourdet M, Juliano MA, Juliano L, Gauthier F, Moreau T. New, sensitive fluorogenic substrates for human cathepsin G based on the sequence of serpin-reactive site loops. <i>J. Biol. Chem.</i>, <b>274</b>, 13810–13817 (1999).

34) Hurt B, Schulick R, Edil B, El Kasmi KC, Barnett C Jr. Cancer-promoting mechanisms of tumor-associated neutrophils. <i>Am. J. Surg.</i>, <b>214</b>, 938–944 (2017).

35) Sato T, Takahashi S, Mizumoto T, Harao M, Akizuki M, Takasugi M, Fukutomi T, Yamashita J. Neutrophil elastase and cancer. <i>Surg. Oncol.</i>, <b>15</b>, 217–222 (2006).

36) Maxwell P, van den Berg HW. Changes in the secretion of insulin-like growth factor binding proteins-2 and -4 associated with the development of tamoxifen resistance and estrogen independence in human breast cancer cell lines. <i>Cancer Lett.</i>, <b>139</b>, 121–127 (1999).

37) Akkiprik M, Nicorici D, Cogdell D, Jia YJ, Hategan A, Tabus I, Yli-Harja O, Yu D, Sahin A, Zhang W. Dissection of signaling pathways in fourteen breast cancer cell lines using reverse-phase protein lysate microarray. <i>Technol. Cancer Res. Treat.</i>, <b>5</b>, 543–551 (2006).

38) Probst-Hensch NM, Steiner JH, Schraml P, Varga Z, Zürrer-Härdi U, Storz M, Korol D, Fehr MK, Fink D, Pestalozzi BC, Lütolf UM, Theurillat JP, Moch H. IGFBP2 and IGFBP3 protein expressions in human breast cancer: association with hormonal factors and obesity. <i>Clin. Cancer Res.</i>, <b>16</b>, 1025–1032 (2010).

39) Ruan W, Kleinberg DL. Insulin-like growth factor I is essential for terminal end bud formation and ductal morphogenesis during mammary development. <i>Endocrinology</i>, <b>140</b>, 5075–5081 (1999).

40) Pollak MN, Schernhammer ES, Hankinson SE. Insulin-like growth factors and neoplasia. <i>Nat. Rev. Cancer</i>, <b>4</b>, 505–518 (2004).

41) Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. <i>Nat. Rev. Cancer</i>, <b>12</b>, 159–169 (2012).

42) Pickard A, McCance DJ. IGF-binding protein 2—oncogene or tumor suppressor? <i>Front. Endocrinol.</i>, <b>6</b>, 25 (2015).

43) Weroha SJ, Haluska P. The insulin-like growth factor system in cancer. <i>Endocrinol. Metab. Clin. North Am.</i>, <b>41</b>, 335–350 (2012).

44) Busund LT, Richardsen E, Busund R, Ukkonen T, Bjørnsen T, Busch C, Stalsberg H. Significant expression of IGFBP2 in breast cancer compared with benign lesions. <i>J. Clin. Pathol.</i>, <b>58</b>, 361–366 (2005).

45) Wang H, Rosen DG, Wang H, Fuller GN, Zhang W, Liu J. Insulin-like growth factor- binding protein 2 and 5 are differentially regulated in ovarian cancer of different histologic types. <i>Mod. Pathol.</i>, <b>19</b>, 1149–1156 (2006).

46) Fukushima T, Kataoka H. Roles of insulin-like growth factor binding protein-2 (IGFBP-2) in glioblastoma. <i>Anticancer Res.</i>, <b>27</b> (6A), 3685–3692 (2007).

47) Azar WJ, Zivkovic S, Werther GA, Russo VC. IGFBP-2 nuclear translocation is mediated by a functional NLS sequence and is essential for its pro-tumorigenic actions in cancer cells. <i>Oncogene</i>, <b>33</b>, 578–588 (2014).