Paclitaxel-induced hypothermia and hypoperfusion increase breast cancer metastasis and angiogenesis in mice

Ami,Nozomi; Sato,Hideki; Hayakawa,Yoshihiro

doi:10.3892/ol.2017.7621

Paclitaxel-induced hypothermia and hypoperfusion increase breast cancer metastasis and angiogenesis in mice

Authors:
- Nozomi Ami
- Hideki Sato
- Yoshihiro Hayakawa
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Affiliations: R&D Center, Terumo Corp., Nakai‑machi, Kanagawa 259‑0151, Japan, Division of Pathogenic Biochemistry, Institute of Natural Medicine, University of Toyama, Toyama‑shi, Toyama 930‑0194, Japan
Published online on: December 14, 2017 https://doi.org/10.3892/ol.2017.7621
Pages: 2330-2334
Copyright: © Ami et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Housing temperature has been shown to influence thermoregulation and behavior of preclinical cancer models; and anti‑cancer drugs typically reduce peripheral blood flow and body temperature. In the present study, the effects of paclitaxel (PTX)‑induced reduction of body temperature and peripheral blood flow on metastatic 4T1 breast cancer was investigated in a mouse model and the modification of these effects by thermoneutral temperature was also assessed. A single dose of PTX decreased the body temperature and peripheral blood flow in mice housed at a standard temperature (23˚C). Furthermore, although lung metastasis and angiogenesis of inoculated 4T1 cells increased in mice pretreated with PTX, mice housed at a thermoneutral temperature (30˚C) could compensate their body temperature and peripheral blood flow compared with control mice, and also suppressed 4T1 angiogenesis and metastasis to lung. The present results imply that maintenance of body temperature or efficient energy supply for thermogenesis may prevent tumor relapse or metastasis after chemotherapy.

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1	Kirchmair R, Tietz AB, Panagiotou E, Walter DH, Silver M, Yoon YS, Schratzberger P, Weber A, Kusano K, Weinberg DH, et al: Therapeutic angiogenesis inhibits or rescues chemotherapy-induced peripheral neuropathy: Taxol- and thalidomide-induced injury of vasa nervorum is ameliorated by VEGF. Mol Ther. 15:69–75. 2007. View Article : Google Scholar : PubMed/NCBI
2	Gauchan P, Andoh T, Kato A, Sasaki A and Kuraishi Y: Effects of the prostaglandin E1 analog limaprost on mechanical allodynia caused by chemotherapeutic agents in mice. J Pharmacol Sci. 109:469–472. 2009. View Article : Google Scholar : PubMed/NCBI
3	Paduch R: The role of lymphangiogenesis and angiogenesis in tumor metastasis. Cell Oncol (Dordr). 39:397–410. 2016. View Article : Google Scholar : PubMed/NCBI
4	Gupta MK and Qin RY: Mechanism and its regulation of tumor-induced angiogenesis. World J Gastroenterol. 9:1144–1155. 2003. View Article : Google Scholar : PubMed/NCBI
5	Vaupel P and Harrison L: Tumor hypoxia: Causative factors, compensatory mechanisms, and cellular response. Oncologist. 9 Suppl 5:S4–S9. 2004. View Article : Google Scholar
6	Muz B, de la Puente P, Azab F and Azab AK: The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckl). 3:83–92. 2015. View Article : Google Scholar : PubMed/NCBI
7	Morfoisse F, Renaud E, Hantelys F, Prats AC and Garmy-Susini B: Role of hypoxia and vascular endothelial growth factors in lymphangiogenesis. Mol Cell Oncol. 2:e10248212015. View Article : Google Scholar : PubMed/NCBI
8	Cao Z, Shang B, Zhang G, Miele L, Sarkar FH, Wang Z and Zhou Q: Tumor cell-mediated neovascularization and lymphangiogenesis contrive tumor progression and cancer metastasis. Biochim Biophys Acta. 1836:273–286. 2013.PubMed/NCBI
9	Guindon J and Hohmann AG: Use of sodium bicarbonate to promote weight gain, maintain body temperature, normalize renal functions and minimize mortality in rodents receiving the chemotherapeutic agent cisplatin. Neurosci Lett. 544:41–46. 2013. View Article : Google Scholar : PubMed/NCBI
10	Guindon J, Deng L, Fan B, Wager-Miller J and Hohmann AG: Optimization of a cisplatin model of chemotherapy-induced peripheral neuropathy in mice: Use of vitamin C and sodium bicarbonate pretreatments to reduce nephrotoxicity and improve animal health status. Mol Pain. 10:562014. View Article : Google Scholar : PubMed/NCBI
11	Fairchild KD, Viscardi RM, Hester L, Singh IS and Hasday JD: Effects of hypothermia and hyperthermia on cytokine production by cultured human mononuclear phagocytes from adults and newborns. J Interf cytokine Res. 20:1049–1055. 2000. View Article : Google Scholar
12	Sahdo B, Evans AL, Arnemo JM, Fröbert O, Särndahl E and Blanc S: Body temperature during hibernation is highly correlated with a decrease in circulating innate immune cells in the brown bear (Ursus arctos): A common feature among hibernators? Int J Med Sci. 10:508–514. 2013. View Article : Google Scholar : PubMed/NCBI
13	Ribatti D: The concept of immune surveillance against tumors. The first theories. Oncotarget. 8:7175–7180. 2017.PubMed/NCBI
14	Peto J: Cancer epidemiology in the last century and the next decade. Nature. 411:390–395. 2001. View Article : Google Scholar : PubMed/NCBI
15	Melvold RW and Sticca RP: Basic and tumor immunology: A review. Surg Oncol Clin N Am. 16(711–735): vii2007.
16	Hylander BL and Repasky EA: Thermoneutrality, mice, and cancer: A heated opinion. Trends Cancer. 2:166–175. 2016. View Article : Google Scholar : PubMed/NCBI
17	Lou C, Takahashi K, Irimura T, Saiki I and Hayakawa Y: Identification of Hirsutine as an anti-metastatic phytochemical by targeting NF-κB activation. Int J Oncol. 45:2085–2091. 2014. View Article : Google Scholar : PubMed/NCBI
18	Suehiro J, Hamakubo T, Kodama T, Aird WC and Minami T: Vascular endothelial growth factor activation of endothelial cells is mediated by early growth response-3. Blood. 115:2520–2532. 2010. View Article : Google Scholar : PubMed/NCBI
19	Lin WL, Wu SK, Chiang CF, Hsu YH, Lin TH, Liou HC, Fu WM and Lin WL: Short-time focused ultrasound hyperthermia enhances liposomal doxorubicin delivery and antitumor efficacy for brain metastasis of breast cancer. Int J Nanomedicine. 9:4485–4494. 2014. View Article : Google Scholar : PubMed/NCBI
20	Alawi KM, Aubdool AA, Liang L, Wilde E, Vepa A, Psefteli MP, Brain SD and Keeble JE: The sympathetic nervous system is controlled by transient receptor potential vanilloid 1 in the regulation of body temperature. FASEB J. 29:4285–4298. 2015. View Article : Google Scholar : PubMed/NCBI
21	Feketa VV and Marrelli SP: Induction of therapeutic hypothermia by pharmacological modulation of temperature-sensitive TRP channels: Theoretical framework and practical considerations. Temperature (Austin). 2:244–257. 2015. View Article : Google Scholar : PubMed/NCBI
22	Morrison SF: Central control of body temperature. F1000Res. 5:pii: F1000. 2016. View Article : Google Scholar : PubMed/NCBI
23	Ootsuka Y and Tanaka M: Control of cutaneous blood flow by central nervous system. Temperature (Austin). 2:392–405. 2015. View Article : Google Scholar : PubMed/NCBI
24	Gadea E, Thivat E, Merlin C, Paulon R, Kwiatkowski F, Chadeyras JB, Coudert B, Boirie Y, Morio B and Durando X: Brown adipose tissue activity in relation to weight gain during chemotherapy in breast cancer patients: A pilot study. Nutr Cancer. 66:1092–1096. 2014. View Article : Google Scholar : PubMed/NCBI
25	Kataoka N, Hioki H, Kaneko T and Nakamura K: Psychological stress activates a dorsomedial hypothalamus-medullary raphe circuit driving brown adipose tissue thermogenesis and hyperthermia. Cell Metab. 20:346–358. 2014. View Article : Google Scholar : PubMed/NCBI
26	Lodhi IJ and Semenkovich CF: Why we should put clothes on mice. Cell Metab. 9:111–112. 2009. View Article : Google Scholar : PubMed/NCBI
27	Kokolus KM, Capitano ML, Lee CT, Eng JW, Waight JD, Hylander BL, Sexton S, Hong CC, Gordon CJ, Abrams SI and Repasky EA: Baseline tumor growth and immune control in laboratory mice are significantly influenced by subthermoneutral housing temperature. Proc Natl Acad Sci USA. 110:20176–20181. 2013. View Article : Google Scholar : PubMed/NCBI
28	Ma YL, Ye J, Zhang PX, Xia XJ and Liu YL: Comparative study on pharmacokinetics and tissue distribution of a novel microemulsion based on the paclitaxel/L-OH lipid complex and paclitaxel injection in cremophor. Yao Xue Xue Bao. 48:1698–1704. 2013.(In Chinese). PubMed/NCBI
29	Ben-Eliyahu S, Shakhar G, Rosenne E, Levinson Y and Beilin B: Hypothermia in barbiturate-anesthetized rats suppresses natural killer cell activity and compromises resistance to tumor metastasis: A role for adrenergic mechanisms. Anesthesiology. 91:732–740. 1999. View Article : Google Scholar : PubMed/NCBI
30	Jürgens HS, Schürmann A, Kluge R, Ortmann S, Klaus S, Joost HG and Tschöp MH: Hyperphagia, lower body temperature, and reduced running wheel activity precede development of morbid obesity in New Zealand obese mice. Physiol Genomics. 25:234–241. 2006. View Article : Google Scholar : PubMed/NCBI
31	Klaus S, Münzberg H, Trüloff C and Heldmaier G: Physiology of transgenic mice with brown fat ablation: Obesity is due to lowered body temperature. Am J Physiol. 274:R287–R293. 1998.PubMed/NCBI
32	Mori A, Sakurai H, Choo MK, Obi R, Koizumi K, Yoshida C, Shimada Y and Saiki I: Severe pulmonary metastasis in obese and diabetic mice. Int J Cancer. 119:2760–2767. 2006. View Article : Google Scholar : PubMed/NCBI
33	Luheshi GN, Gardner JD, Rushforth DA, Loudon AS and Rothwell NJ: Leptin actions on food intake and body temperature are mediated by IL-1. Proc Natl Acad Sci USA. 96:7047–7052. 1999. View Article : Google Scholar : PubMed/NCBI
34	Kon K, Maeda N and Shiga T: Erythrocyte deformation in shear flow: Influences of internal viscosity, membrane stiffness, and hematocrit. Blood. 69:727–734. 1987.PubMed/NCBI
35	Mitchell MJ and King MR: Fluid shear stress sensitizes cancer cells to receptor-mediated apoptosis via trimeric death receptors. New J Phys. 15:150082013. View Article : Google Scholar