Open Access

Advances in glucose metabolism research in colorectal cancer (Review)

  • Authors:
    • Sitian Fang
    • Xiao Fang
  • View Affiliations

  • Published online on: July 18, 2016     https://doi.org/10.3892/br.2016.719
  • Pages: 289-295
  • Copyright: © Fang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Cancer cells uptake glucose at a higher rate and produce lactic acid rather than metabolizing pyruvate through the tricarboxylic acid cycle. This adaptive metabolic shift is termed the Warburg effect. Recently progress had been made regarding the mechanistic understanding of glucose metabolism and associated diagnostic and therapeutic methods, which have been investigated in colorectal cancer. The majority of novel mechanisms involve important glucose metabolism associated genes and miRNA regulation. The present review discusses the contribution of these research results to facilitate with the development of novel diagnosis and anticancer treatment options.

References

1 

Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global patterns and trends in colorectal cancer incidence and mortality. Gut. Jan 27–2016.(Epub ahead of print). doi: 10.1136/gutjnl-2015-310912. View Article : Google Scholar

2 

Cerella C, Gaigneaux A, Dicato M and Diederich M: Antagonistic role of natural compounds in mTOR-mediated metabolic reprogramming. Cancer Lett. 356:251–262. 2015. View Article : Google Scholar : PubMed/NCBI

3 

Cerella C, Radogna F, Dicato M and Diederich M: Natural compounds as regulators of the cancer cell metabolism. Int J Cell Biol. 2013:6394012013. View Article : Google Scholar : PubMed/NCBI

4 

Cerella C, Michiels C, Dashwood RH, Surh YJ and Diederich M: Metabolism and cancer: old and new players. Int J Cell Biol. 2013:2932012013. View Article : Google Scholar : PubMed/NCBI

5 

Cairns RA, Harris IS and Mak TW: Regulation of cancer cell metabolism. Nat Rev Cancer. 11:85–95. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Rasheed S, Harris AL, Tekkis PP, Turley H, Silver A, McDonald PJ, Talbot IC, Glynne-Jones R, Northover JM and Guenther T: Hypoxia-inducible factor-1alpha and −2alpha are expressed in most rectal cancers but only hypoxia-inducible factor-1alpha is associated with prognosis. Br J Cancer. 100:1666–1673. 2009. View Article : Google Scholar : PubMed/NCBI

7 

Yoshimura H, Dhar DK, Kohno H, Kubota H, Fujii T, Ueda S, Kinugasa S, Tachibana M and Nagasue N: Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clin Cancer Res. 10:8554–8560. 2004. View Article : Google Scholar : PubMed/NCBI

8 

Schmitz KJ, Müller CI, Reis H, Alakus H, Winde G, Baba HA, Wohlschlaeger J, Jasani B, Fandrey J and Schmid KW: Combined analysis of hypoxia-inducible factor 1 alpha and metallothionein indicates an aggressive subtype of colorectal carcinoma. Int J Colorectal Dis. 24:1287–1296. 2009. View Article : Google Scholar : PubMed/NCBI

9 

Rajaganeshan R, Prasad R, Guillou PJ, Scott N, Poston G and Jayne DG: Expression patterns of hypoxic markers at the invasive margin of colorectal cancers and liver metastases. Eur J Surg Oncol. 35:1286–1294. 2009. View Article : Google Scholar : PubMed/NCBI

10 

Kuwai T, Kitadai Y, Tanaka S, Onogawa S, Matsutani N, Kaio E, Ito M and Chayama K: Expression of hypoxia-inducible factor-1alpha is associated with tumor vascularization in human colorectal carcinoma. Int J Cancer. 105:176–181. 2003. View Article : Google Scholar : PubMed/NCBI

11 

Furlan D, Sahnane N, Carnevali I, Cerutti R, Bertoni F, Kwee I, Uccella S, Bertolini V, Chiaravalli AM and Capella C: Up-regulation of the hypoxia-inducible factor-1 transcriptional pathway in colorectal carcinomas. Hum Pathol. 39:1483–1494. 2008. View Article : Google Scholar : PubMed/NCBI

12 

Baba Y, Nosho K, Shima K, Irahara N, Chan AT, Meyerhardt JA, Chung DC, Giovannucci EL, Fuchs CS and Ogino S: HIF1A overexpression is associated with poor prognosis in a cohort of 731 colorectal cancers. Am J Pathol. 176:2292–2301. 2010. View Article : Google Scholar : PubMed/NCBI

13 

Wang H, Zhao L, Zhu LT, Wang Y, Pan D, Yao J, You QD and Guo QL: Wogonin reverses hypoxia resistance of human colon cancer HCT116 cells via downregulation of HIF-1α and glycolysis, by inhibiting PI3K/Akt signaling pathway. Mol Carcinog. 53(Suppl 1): E107–E118. 2014. View Article : Google Scholar : PubMed/NCBI

14 

Kozutsumi Y, Segal M, Normington K, Gething MJ and Sambrook J: The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 332:462–464. 1988. View Article : Google Scholar : PubMed/NCBI

15 

Xing X, Lai M, Wang Y, Xu E and Huang Q: Overexpression of glucose-regulated protein 78 in colon cancer. Clin Chim Acta. 364:308–315. 2006. View Article : Google Scholar : PubMed/NCBI

16 

Takahashi H, Wang JP, Zheng HC, Masuda S and Takano Y: Overexpression of GRP78 and GRP94 is involved in colorectal carcinogenesis. Histol Histopathol. 26:663–671. 2011.PubMed/NCBI

17 

Huang CY, Kuo WT, Huang YC, Lee TC and Yu LC: Resistance to hypoxia-induced necroptosis is conferred by glycolytic pyruvate scavenging of mitochondrial superoxide in colorectal cancer cells. Cell Death Dis. 4:e6222013. View Article : Google Scholar : PubMed/NCBI

18 

Younes M, Lechago LV and Lechago J: Overexpression of the human erythrocyte glucose transporter occurs as a late event in human colorectal carcinogenesis and is associated with an increased incidence of lymph node metastases. Clin Cancer Res. 2:1151–1154. 1996.PubMed/NCBI

19 

Haber RS, Rathan A, Weiser KR, Pritsker A, Itzkowitz SH, Bodian C, Slater G, Weiss A and Burstein DE: GLUT1 glucose transporter expression in colorectal carcinoma: A marker for poor prognosis. Cancer. 83:34–40. 1998. View Article : Google Scholar : PubMed/NCBI

20 

Korkeila E, Jaakkola PM, Syrjänen K, Pyrhönen S and Sundström J: Pronounced tumour regression after radiotherapy is associated with negative/weak glucose transporter-1 expression in rectal cancer. Anticancer Res. 31:311–315. 2011.PubMed/NCBI

21 

Wang W, Xiao ZD, Li X, Aziz KE, Gan B, Johnson RL and Chen J: AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat Cell Biol. 17:490–499. 2015. View Article : Google Scholar : PubMed/NCBI

22 

Li QQ, Sun YP, Ruan CP, Xu XY, Ge JH, He J, Xu ZD, Wang Q and Gao WC: Cellular prion protein promotes glucose uptake through the Fyn-HIF-2α-Glut1 pathway to support colorectal cancer cell survival. Cancer Sci. 102:400–406. 2011. View Article : Google Scholar : PubMed/NCBI

23 

Song HT, Qin Y, Yao GD, Tian ZN, Fu SB and Geng JS: Astrocyte elevated gene-1 mediates glycolysis and tumorigenesis in colorectal carcinoma cells via AMPK signaling. Mediators Inflamm. 2014:2873812014. View Article : Google Scholar : PubMed/NCBI

24 

Qiu SL, Xiao ZC, Piao CM, Xian YL, Jia LX, Qi YF, Han JH, Zhang YY and Du J: AMP-activated protein kinase α2 protects against liver injury from metastasized tumors via reduced glucose deprivation-induced oxidative stress. J Biol Chem. 289:9449–9459. 2014. View Article : Google Scholar : PubMed/NCBI

25 

Nam SO, Yotsumoto F, Miyata K, Fukagawa S, Yamada H, Kuroki M and Miyamoto S: Warburg effect regulated by amphiregulin in the development of colorectal cancer. Cancer Med. 4:575–587. 2015. View Article : Google Scholar : PubMed/NCBI

26 

Tambe Y, Hasebe M, Kim CJ, Yamamoto A and Inoue H: The drs tumor suppressor regulates glucose metabolism via lactate dehydrogenase-B. Mol Carcinog. 55:52–63. 2016. View Article : Google Scholar : PubMed/NCBI

27 

Bernatchez G, Giroux V, Lassalle T, Carpentier AC, Rivard N and Carrier JC: ERRα metabolic nuclear receptor controls growth of colon cancer cells. Carcinogenesis. 34:2253–2261. 2013. View Article : Google Scholar : PubMed/NCBI

28 

Pate KT, Stringari C, Sprowl-Tanio S, Wang K, TeSlaa T, Hoverter NP, McQuade MM, Garner C, Digman MA, Teitell MA, et al: Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer. EMBO J. 33:1454–1473. 2014.PubMed/NCBI

29 

Diaz-Moralli S, Tarrado-Castellarnau M, Alenda C, Castells A and Cascante M: Transketolase-like 1 expression is modulated during colorectal cancer progression and metastasis formation. PLoS One. 6:e253232011. View Article : Google Scholar : PubMed/NCBI

30 

Harrison RA: The detection of hexokinase, glucosephosphate isomerase and phosphoglucomutase activities in polyacrylamide gels after electrophoresis: a novel method using immobilized glucose 6-phosphate dehydrogenase. Anal Biochem. 61:500–507. 1974. View Article : Google Scholar : PubMed/NCBI

31 

Tsutsumi S, Fukasawa T, Yamauchi H, Kato T, Kigure W, Morita H, Asao T and Kuwano H: Phosphoglucose isomerase enhances colorectal cancer metastasis. Int J Oncol. 35:1117–1121. 2009. View Article : Google Scholar : PubMed/NCBI

32 

Ha TK and Chi SG: CAV1/caveolin 1 enhances aerobic glycolysis in colon cancer cells via activation of SLC2A3/GLUT3 transcription. Autophagy. 8:1684–1685. 2012. View Article : Google Scholar : PubMed/NCBI

33 

Tong X, Zhao F, Mancuso A, Gruber JJ and Thompson CB: The glucose-responsive transcription factor ChREBP contributes to glucose-dependent anabolic synthesis and cell proliferation. Proc Natl Acad Sci USA. 106:21660–21665. 2009. View Article : Google Scholar : PubMed/NCBI

34 

Ericson NG, Kulawiec M, Vermulst M, Sheahan K, O'Sullivan J, Salk JJ and Bielas JH: Decreased mitochondrial DNA mutagenesis in human colorectal cancer. PLoS Genet. 8:e10026892012. View Article : Google Scholar : PubMed/NCBI

35 

Yun J, Rago C, Cheong I, Pagliarini R, Angenendt P, Rajagopalan H, Schmidt K, Willson JK, Markowitz S, Zhou S, et al: Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science. 325:1555–1559. 2009. View Article : Google Scholar : PubMed/NCBI

36 

Straus DS: TNFα and IL-17 cooperatively stimulate glucose metabolism and growth factor production in human colorectal cancer cells. Mol Cancer. 12:782013. View Article : Google Scholar : PubMed/NCBI

37 

Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, Moretti M, De Smaele E, Beg AA, Tergaonkar V, et al: NF-κB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol. 13:1272–1279. 2011. View Article : Google Scholar : PubMed/NCBI

38 

Pucci S and Mazzarelli P: MicroRNA dysregulation in colon cancer microenvironment interactions: the importance of small things in metastases. Cancer Microenviron. 4:155–162. 2011. View Article : Google Scholar : PubMed/NCBI

39 

Fang R, Xiao T, Fang Z, Sun Y, Li F, Gao Y, Feng Y, Li L, Wang Y, Liu X, et al: MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J Biol Chem. 287:23227–23235. 2012. View Article : Google Scholar : PubMed/NCBI

40 

Singh PK, Brand RE and Mehla K: MicroRNAs in pancreatic cancer metabolism. Nat Rev Gastroenterol Hepatol. 9:334–344. 2012. View Article : Google Scholar : PubMed/NCBI

41 

Chen B, Liu Y, Jin X, Lu W, Liu J, Xia Z, Yuan Q, Zhao X, Xu N and Liang S: MicroRNA-26a regulates glucose metabolism by direct targeting PDHX in colorectal cancer cells. BMC Cancer. 14:4432014. View Article : Google Scholar : PubMed/NCBI

42 

Gregersen LH, Jacobsen A, Frankel LB, Wen J, Krogh A and Lund AH: MicroRNA-143 down-regulates Hexokinase 2 in colon cancer cells. BMC Cancer. 12:2322012. View Article : Google Scholar : PubMed/NCBI

43 

Sun Y, Zhao X, Luo M, Zhou Y, Ren W, Wu K, Li X, Shen J and Hu Y: The pro-apoptotic role of the regulatory feedback loop between miR-124 and PKM1/HNF4α in colorectal cancer cells. Int J Mol Sci. 15:4318–4332. 2014. View Article : Google Scholar : PubMed/NCBI

44 

Sun Y, Zhao X, Zhou Y and Hu Y: miR-124, miR-137 and miR-340 regulate colorectal cancer growth via inhibition of the Warburg effect. Oncol Rep. 28:1346–1352. 2012.PubMed/NCBI

45 

Wang J, Wang H, Liu A, Fang C, Hao J and Wang Z: Lactate dehydrogenase A negatively regulated by miRNAs promotes aerobic glycolysis and is increased in colorectal cancer. Oncotarget. 6:19456–19468. 2015. View Article : Google Scholar : PubMed/NCBI

46 

He J, Xie G, Tong J, Peng Y, Huang H, Li J, Wang N and Liang H: Overexpression of microRNA-122 re-sensitizes 5-FU-resistant colon cancer cells to 5-FU through the inhibition of PKM2 in vitro and in vivo. Cell Biochem Biophys. 70:1343–1350. 2014. View Article : Google Scholar : PubMed/NCBI

47 

Li X, Zhao H, Zhou X and Song L: Inhibition of lactate dehydrogenase A by microRNA-34a resensitizes colon cancer cells to 5-fluorouracil. Mol Med Rep. 11:577–582. 2015.PubMed/NCBI

48 

Ellis BC, Graham LD and Molloy PL: CRNDE, a long non-coding RNA responsive to insulin/IGF signaling, regulates genes involved in central metabolism. Biochim Biophys Acta. 1843:372–386. 2014. View Article : Google Scholar : PubMed/NCBI

49 

Taniguchi K, Sugito N, Kumazaki M, Shinohara H, Yamada N, Nakagawa Y, Ito Y, Otsuki Y, Uno B, Uchiyama K, et al: MicroRNA-124 inhibits cancer cell growth through PTB1/PKM1/PKM2 feedback cascade in colorectal cancer. Cancer Lett. 363:17–27. 2015. View Article : Google Scholar : PubMed/NCBI

50 

Taniguchi K, Sugito N, Kumazaki M, Shinohara H, Yamada N, Matsuhashi N, Futamura M, Ito Y, Otsuki Y, Yoshida K, et al: Positive feedback of DDX6/c-Myc/PTB1 regulated by miR-124 contributes to maintenance of the Warburg effect in colon cancer cells. Biochim Biophys Acta. 1852:1971–1980. 2015. View Article : Google Scholar : PubMed/NCBI

51 

Xu X, Zur Hausen A, Coy JF and Löchelt M: Transketolase-like protein 1 (TKTL1) is required for rapid cell growth and full viability of human tumor cells. Int J Cancer. 124:1330–1337. 2009. View Article : Google Scholar : PubMed/NCBI

52 

Shibuya N, Inoue K, Tanaka G, Akimoto K and Kubota K: Augmented pentose phosphate pathway plays critical roles in colorectal carcinomas. Oncology. 88:309–319. 2015. View Article : Google Scholar : PubMed/NCBI

53 

Ma L, Tao Y, Duran A, Llado V, Galvez A, Barger JF, Castilla EA, Chen J, Yajima T, Porollo A, et al: Control of nutrient stress-induced metabolic reprogramming by PKCζ in tumorigenesis. Cell. 152:599–611. 2013. View Article : Google Scholar : PubMed/NCBI

54 

Duffy MJ: Carcinoembryonic antigen as a marker for colorectal cancer: Is it clinically useful? Clin Chem. 47:624–630. 2001.PubMed/NCBI

55 

Culverwell AD, Chowdhury FU and Scarsbrook AF: Optimizing the role of FDG PET-CT for potentially operable metastatic colorectal cancer. Abdom Imaging. 37:1021–1031. 2012. View Article : Google Scholar : PubMed/NCBI

56 

Xing X, Zhang B, Wang X, Liu F, Shi D and Cheng Y: An ‘imaging-biopsy’ strategy for colorectal tumor reconfirmation by multipurpose paramagnetic quantum dots. Biomaterials. 48:16–25. 2015. View Article : Google Scholar : PubMed/NCBI

57 

Sánchez-Aragó M and Cuezva JM: The bioenergetic signature of isogenic colon cancer cells predicts the cell death response to treatment with 3-bromopyruvate, iodoacetate or 5-fluorouracil. J Transl Med. 9:192011. View Article : Google Scholar : PubMed/NCBI

58 

Omar HA, Berman-Booty L and Weng JR: Energy restriction: stepping stones towards cancer therapy. Future Oncol. 8:1503–1506. 2012. View Article : Google Scholar : PubMed/NCBI

59 

Hursting SD, Dunlap SM, Ford NA, Hursting MJ and Lashinger LM: Calorie restriction and cancer prevention: Α mechanistic perspective. Cancer Metab. 1:102013. View Article : Google Scholar : PubMed/NCBI

60 

Chen GQ, Tang CF, Shi XK, Lin CY, Fatima S, Pan XH, Yang DJ, Zhang G, Lu AP, Lin SH, et al: Halofuginone inhibits colorectal cancer growth through suppression of Akt/mTORC1 signaling and glucose metabolism. Oncotarget. 6:24148–24162. 2015. View Article : Google Scholar : PubMed/NCBI

61 

Arafa SA, Abdelazeem AH, Arab HH and Omar HA: OSU-CG5, a novel energy restriction mimetic agent, targets human colorectal cancer cells in vitro. Acta Pharmacol Sin. 35:394–400. 2014. View Article : Google Scholar : PubMed/NCBI

62 

Zwicker F, Kirsner A, Peschke P, Roeder F, Debus J, Huber PE and Weber KJ: Dichloroacetate induces tumor-specific radiosensitivity in vitro but attenuates radiation-induced tumor growth delay in vivo. Strahlenther Onkol. 189:684–692. 2013. View Article : Google Scholar : PubMed/NCBI

63 

Fath MA, Diers AR, Aykin-Burns N, Simons AL, Hua L and Spitz DR: Mitochondrial electron transport chain blockers enhance 2-deoxy-D-glucose induced oxidative stress and cell killing in human colon carcinoma cells. Cancer Biol Ther. 8:1228–1236. 2009. View Article : Google Scholar : PubMed/NCBI

64 

Ying Q, Ansong E, Diamond AM, Lu Z, Yang W and Bie X: Quantitative proteomic analysis reveals that anti-cancer effects of selenium-binding protein 1 in vivo are associated with metabolic pathways. PLoS One. 10:e01262852015. View Article : Google Scholar : PubMed/NCBI

65 

Marimuthu S, Chivukula RS, Alfonso LF, Moridani M, Hagen FK and Bhat GJ: Aspirin acetylates multiple cellular proteins in HCT-116 colon cancer cells: identification of novel targets. Int J Oncol. 39:1273–1283. 2011.PubMed/NCBI

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Copy and paste a formatted citation
APA
Fang, S., & Fang, S. (2016). Advances in glucose metabolism research in colorectal cancer (Review). Biomedical Reports, 5, 289-295. https://doi.org/10.3892/br.2016.719
MLA
Fang, S., Fang, X."Advances in glucose metabolism research in colorectal cancer (Review)". Biomedical Reports 5.3 (2016): 289-295.
Chicago
Fang, S., Fang, X."Advances in glucose metabolism research in colorectal cancer (Review)". Biomedical Reports 5, no. 3 (2016): 289-295. https://doi.org/10.3892/br.2016.719