Optical redox ratio identifies metastatic potential-dependent changes in breast cancer cell metabolism

The development of prognostic indicators of breast cancer metastatic risk could reduce the number of patients receiving chemotherapy for tumors with low metastatic potential. Recent evidence points to a critical role for cell metabolism in driving breast cancer metastasis. Endogenous fluorescence in...

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Published inBiomedical optics express Vol. 7; no. 11; pp. 4364 - 4374
Main Authors Alhallak, Kinan, Rebello, Lisa G, Muldoon, Timothy J, Quinn, Kyle P, Rajaram, Narasimhan
Format Journal Article
LanguageEnglish
Published United States Optical Society of America 01.11.2016
Subjects
(170.2655) Functional monitoring and imaging
(170.1530) Cell analysis
(170.2520) Fluorescence microscopy
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Abstract The development of prognostic indicators of breast cancer metastatic risk could reduce the number of patients receiving chemotherapy for tumors with low metastatic potential. Recent evidence points to a critical role for cell metabolism in driving breast cancer metastasis. Endogenous fluorescence intensity of nicotinamide adenine dinucleotide (NADH) and flavin adenine dinucleotide (FAD) can provide a label-free method for assessing cell metabolism. We report the optical redox ratio of FAD/(FAD + NADH) of four isogenic triple-negative breast cancer cell lines with varying metastatic potential. Under normoxic conditions, the redox ratio increases with increasing metastatic potential (168FARN>4T07>4T1), indicating a shift to more oxidative metabolism in cells capable of metastasis. Reoxygenation following acute hypoxia increased the redox ratio by 43 ± 9% and 33 ± 4% in the 4T1 and 4T07 cells, respectively; in contrast, the redox ratio decreased 14 ± 7% in the non-metastatic 67NR cell line. These results demonstrate that the optical redox ratio is sensitive to the metabolic adaptability of breast cancer cells with high metastatic potential and could potentially be used to measure dynamic functional changes that are indicative of invasive or metastatic potential.
AbstractList The development of prognostic indicators of breast cancer metastatic risk could reduce the number of patients receiving chemotherapy for tumors with low metastatic potential. Recent evidence points to a critical role for cell metabolism in driving breast cancer metastasis. Endogenous fluorescence intensity of nicotinamide adenine dinucleotide (NADH) and flavin adenine dinucleotide (FAD) can provide a label-free method for assessing cell metabolism. We report the optical redox ratio of FAD/(FAD + NADH) of four isogenic triple-negative breast cancer cell lines with varying metastatic potential. Under normoxic conditions, the redox ratio increases with increasing metastatic potential (168FARN>4T07>4T1), indicating a shift to more oxidative metabolism in cells capable of metastasis. Reoxygenation following acute hypoxia increased the redox ratio by 43 ± 9% and 33 ± 4% in the 4T1 and 4T07 cells, respectively; in contrast, the redox ratio decreased 14 ± 7% in the non-metastatic 67NR cell line. These results demonstrate that the optical redox ratio is sensitive to the metabolic adaptability of breast cancer cells with high metastatic potential and could potentially be used to measure dynamic functional changes that are indicative of invasive or metastatic potential.
Author Alhallak, Kinan
Rajaram, Narasimhan
Quinn, Kyle P
Rebello, Lisa G
Muldoon, Timothy J
Author_xml – sequence: 1
  givenname: Kinan
  surname: Alhallak
  fullname: Alhallak, Kinan
  organization: Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR 72701, USA
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  givenname: Lisa G
  surname: Rebello
  fullname: Rebello, Lisa G
  organization: Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR 72701, USA
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  givenname: Timothy J
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  surname: Quinn
  fullname: Quinn, Kyle P
  organization: Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR 72701, USA
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  givenname: Narasimhan
  surname: Rajaram
  fullname: Rajaram, Narasimhan
  organization: Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR 72701, USA
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Cites_doi 10.1371/journal.pone.0004592
10.1373/clinchem.2006.076497
10.1016/j.cmet.2015.08.007
10.1364/BOE.3.000075
10.1016/j.cell.2004.06.006
10.1117/1.3431714
10.1158/0008-5472.CAN-13-2713
10.1016/j.freeradbiomed.2011.08.005
10.1016/0304-4165(85)90064-9
10.1158/0008-5472.CAN-14-0663
10.1016/j.celrep.2014.06.043
10.1158/0008-5472.CAN-16-0266
10.18632/oncotarget.2285
10.1152/jappl.2000.89.1.169
10.1073/pnas.0901807106
10.1158/0008-5472.CAN-03-2958
10.1126/science.137.3529.499
10.1097/MPA.0000000000000543
10.1038/srep03432
10.1016/j.biomaterials.2012.04.024
10.1158/0008-5472.CAN-13-0527
10.1016/j.ijrobp.2011.04.027
10.1158/0008-5472.CAN-09-2572
10.1117/1.JBO.17.4.046010
10.1158/0008-5472.CAN-03-3196
10.1074/jbc.C110.104448
10.1158/0008-5472.CAN-04-3031
10.1073/pnas.0708425104
10.1016/j.neo.2015.08.005
10.1186/bcr2773
10.1200/JCO.2015.65.8609
10.1016/S0021-9258(17)30079-0
10.1371/journal.pone.0090746
10.1073/pnas.92.12.5510
10.1016/S0140-6736(11)61625-5
10.1038/ncb3039
10.1562/0031-8655(2001)0730636AMOFCT2.0.CO2
10.1364/OE.8.000335
10.1117/1.JBO.21.6.060503
10.1364/BOE.6.000559
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References 26495796 - Pancreas. 2016 Jul;45(6):863-9
15026343 - Cancer Res. 2004 Mar 15;64(6):2054-61
18042710 - Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19494-9
24595244 - PLoS One. 2014 Mar 04;9(3):e90746
27587539 - Cancer Res. 2016 Sep 15;76(18):5201-8
24686167 - Cancer Res. 2014 Jun 1;74(11):3067-75
27001586 - J Clin Oncol. 2016 Jul 1;34(19):2303-11
10904049 - J Appl Physiol (1985). 2000 Jul;89(1):169-75
12810678 - Cancer Res. 2003 Jun 15;63(12):3413-7
27300321 - J Biomed Opt. 2016 Jun 1;21(6):60503
25780745 - Biomed Opt Express. 2015 Jan 15;6(2):559-73
22152853 - Lancet. 2012 Feb 4;379(9814):432-44
4027266 - Biochim Biophys Acta. 1985 Sep 6;841(3):237-46
20139083 - J Biol Chem. 2010 Mar 26;285(13):9317-21
24130112 - Cancer Res. 2013 Oct 15;73(20):6164-74
220260 - J Biol Chem. 1979 Jun 10;254(11):4764-71
22560200 - Biomaterials. 2012 Jul;33(21):5341-8
25100563 - Cancer Res. 2014 Sep 15;74(18):5184-94
1540948 - Cancer Res. 1992 Mar 15;52(6):1399-405
8968110 - Cancer Res. 1996 Dec 1;56(23):5522-8
20072916 - Methods Mol Biol. 2010;594:155-62
17463177 - Clin Chem. 2007 Jun;53(6):1084-91
19366661 - Proc Natl Acad Sci U S A. 2009 Apr 21;106(16):6608-13
7539918 - Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5510-4
3791244 - Cancer Res. 1987 Jan 15;47(2):597-601
21872656 - Free Radic Biol Med. 2011 Nov 1;51(9):1621-35
11751415 - Cancer Res. 2001 Dec 15;61(24):8903-8
22559688 - J Biomed Opt. 2012 Apr;17(4):046010
11421069 - Photochem Photobiol. 2001 Jun;73(6):636-41
25216520 - Oncotarget. 2014 Aug 30;5(16):6947-63
24305550 - Sci Rep. 2013 Dec 05;3:3432
21067584 - Breast Cancer Res. 2010;12(6):R94
25066121 - Cell Rep. 2014 Aug 7;8(3):754-66
22254170 - Biomed Opt Express. 2012 Jan 1;3(1):75-85
21640519 - Int J Radiat Oncol Biol Phys. 2011 Oct 1;81(2):521-8
13878016 - Science. 1962 Aug 17;137(3529):499-508
19240798 - PLoS One. 2009;4(2):e4592
15735001 - Cancer Res. 2005 Feb 15;65(4):1180-6
26365179 - Cell Metab. 2015 Oct 6;22(4):577-89
16489024 - Cancer Res. 2006 Feb 15;66(4):2219-23
26408259 - Neoplasia. 2015 Aug;17(8):671-84
25241037 - Nat Cell Biol. 2014 Oct;16(10 ):992-1003, 1-15
19417824 - Opt Express. 2001 Mar 12;8(6):335-43
20460512 - Cancer Res. 2010 Jun 1;70(11):4759-66
15210113 - Cell. 2004 Jun 25;117(7):927-39
20615012 - J Biomed Opt. 2010 May-Jun;15(3):036010
Walsh (boe-7-11-4364-R32) 2015; 6
Li (boe-7-11-4364-R34) 2009; 106
Dai (boe-7-11-4364-R31) 2011; 81
Yang (boe-7-11-4364-R27) 2004; 117
Skala (boe-7-11-4364-R17) 2005; 65
Simões (boe-7-11-4364-R28) 2015; 17
LeBleu (boe-7-11-4364-R9) 2014; 16
Ostrander (boe-7-11-4364-R20) 2010; 70
Lin (boe-7-11-4364-R4) 2003; 63
Chance (boe-7-11-4364-R11) 1962; 137
Xu (boe-7-11-4364-R25) 2010; 15
Cronin (boe-7-11-4364-R3) 2007; 53
Groussard (boe-7-11-4364-R5) 2000; 89
Porporato (boe-7-11-4364-R8) 2014; 8
Dupuy (boe-7-11-4364-R10) 2015; 22
Chaplin (boe-7-11-4364-R37) 1987; 47
Kimura (boe-7-11-4364-R38) 1996; 56
Walsh (boe-7-11-4364-R33) 2016; 45
Kunz (boe-7-11-4364-R35) 1985; 841
Boidot (boe-7-11-4364-R43) 2014; 5
Aslakson (boe-7-11-4364-R26) 1992; 52
Peto (boe-7-11-4364-R2) 2012; 379
Dranka (boe-7-11-4364-R29) 2011; 51
Chance (boe-7-11-4364-R12) 1979; 254
Wang (boe-7-11-4364-R36) 1995; 92
Cairns (boe-7-11-4364-R42) 2001; 61
Sepehr (boe-7-11-4364-R44) 2012; 17
Shah (boe-7-11-4364-R23) 2014; 9
Lanzen (boe-7-11-4364-R39) 2006; 66
Ramanujam (boe-7-11-4364-R15) 2001; 8
Henry (boe-7-11-4364-R1) 2016; 34
Varone (boe-7-11-4364-R19) 2014; 74
Walsh (boe-7-11-4364-R22) 2013; 73
Quinn (boe-7-11-4364-R13) 2013; 3
Drezek (boe-7-11-4364-R16) 2001; 73
Walsh (boe-7-11-4364-R24) 2014; 74
Louie (boe-7-11-4364-R40) 2010; 12
Lu (boe-7-11-4364-R7) 2010; 285
Cairns (boe-7-11-4364-R41) 2004; 64
Walsh (boe-7-11-4364-R21) 2012; 3
Hou (boe-7-11-4364-R30) 2016; 21
Ruckenstuhl (boe-7-11-4364-R6) 2009; 4
Lehuédé (boe-7-11-4364-R45) 2016; 76
Skala (boe-7-11-4364-R18) 2007; 104
Quinn (boe-7-11-4364-R14) 2012; 33
References_xml – volume: 4
  start-page: e4592
  year: 2009
  ident: boe-7-11-4364-R6
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0004592
  contributor:
    fullname: Ruckenstuhl
– volume: 53
  start-page: 1084
  year: 2007
  ident: boe-7-11-4364-R3
  publication-title: Clin. Chem.
  doi: 10.1373/clinchem.2006.076497
  contributor:
    fullname: Cronin
– volume: 22
  start-page: 577
  year: 2015
  ident: boe-7-11-4364-R10
  publication-title: Cell Metab.
  doi: 10.1016/j.cmet.2015.08.007
  contributor:
    fullname: Dupuy
– volume: 3
  start-page: 75
  year: 2012
  ident: boe-7-11-4364-R21
  publication-title: Biomed. Opt. Express
  doi: 10.1364/BOE.3.000075
  contributor:
    fullname: Walsh
– volume: 117
  start-page: 927
  year: 2004
  ident: boe-7-11-4364-R27
  publication-title: Cell
  doi: 10.1016/j.cell.2004.06.006
  contributor:
    fullname: Yang
– volume: 56
  start-page: 5522
  year: 1996
  ident: boe-7-11-4364-R38
  publication-title: Cancer Res.
  contributor:
    fullname: Kimura
– volume: 15
  start-page: 036010
  year: 2010
  ident: boe-7-11-4364-R25
  publication-title: J. Biomed. Opt.
  doi: 10.1117/1.3431714
  contributor:
    fullname: Xu
– volume: 61
  start-page: 8903
  year: 2001
  ident: boe-7-11-4364-R42
  publication-title: Cancer Res.
  contributor:
    fullname: Cairns
– volume: 63
  start-page: 3413
  year: 2003
  ident: boe-7-11-4364-R4
  publication-title: Cancer Res.
  contributor:
    fullname: Lin
– volume: 74
  start-page: 3067
  year: 2014
  ident: boe-7-11-4364-R19
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-13-2713
  contributor:
    fullname: Varone
– volume: 51
  start-page: 1621
  year: 2011
  ident: boe-7-11-4364-R29
  publication-title: Free Radic. Biol. Med.
  doi: 10.1016/j.freeradbiomed.2011.08.005
  contributor:
    fullname: Dranka
– volume: 841
  start-page: 237
  year: 1985
  ident: boe-7-11-4364-R35
  publication-title: Biochimica et Biophysica Acta (BBA)- General Subjects
  doi: 10.1016/0304-4165(85)90064-9
  contributor:
    fullname: Kunz
– volume: 74
  start-page: 5184
  year: 2014
  ident: boe-7-11-4364-R24
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-14-0663
  contributor:
    fullname: Walsh
– volume: 8
  start-page: 754
  year: 2014
  ident: boe-7-11-4364-R8
  publication-title: Cell Reports
  doi: 10.1016/j.celrep.2014.06.043
  contributor:
    fullname: Porporato
– volume: 76
  start-page: 5201
  year: 2016
  ident: boe-7-11-4364-R45
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-16-0266
  contributor:
    fullname: Lehuédé
– volume: 5
  start-page: 6947
  year: 2014
  ident: boe-7-11-4364-R43
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.2285
  contributor:
    fullname: Boidot
– volume: 47
  start-page: 597
  year: 1987
  ident: boe-7-11-4364-R37
  publication-title: Cancer Res.
  contributor:
    fullname: Chaplin
– volume: 89
  start-page: 169
  year: 2000
  ident: boe-7-11-4364-R5
  publication-title: J. Appl. Physiol.
  doi: 10.1152/jappl.2000.89.1.169
  contributor:
    fullname: Groussard
– volume: 106
  start-page: 6608
  year: 2009
  ident: boe-7-11-4364-R34
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0901807106
  contributor:
    fullname: Li
– volume: 66
  start-page: 2219
  year: 2006
  ident: boe-7-11-4364-R39
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-03-2958
  contributor:
    fullname: Lanzen
– volume: 137
  start-page: 499
  year: 1962
  ident: boe-7-11-4364-R11
  publication-title: Science
  doi: 10.1126/science.137.3529.499
  contributor:
    fullname: Chance
– volume: 45
  start-page: 863
  year: 2016
  ident: boe-7-11-4364-R33
  publication-title: Pancreas
  doi: 10.1097/MPA.0000000000000543
  contributor:
    fullname: Walsh
– volume: 3
  start-page: 3432
  year: 2013
  ident: boe-7-11-4364-R13
  publication-title: Sci. Rep.
  doi: 10.1038/srep03432
  contributor:
    fullname: Quinn
– volume: 33
  start-page: 5341
  year: 2012
  ident: boe-7-11-4364-R14
  publication-title: Biomaterials
  doi: 10.1016/j.biomaterials.2012.04.024
  contributor:
    fullname: Quinn
– volume: 73
  start-page: 6164
  year: 2013
  ident: boe-7-11-4364-R22
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-13-0527
  contributor:
    fullname: Walsh
– volume: 81
  start-page: 521
  year: 2011
  ident: boe-7-11-4364-R31
  publication-title: Int. J. Radiat. Oncol. Biol. Phys.
  doi: 10.1016/j.ijrobp.2011.04.027
  contributor:
    fullname: Dai
– volume: 70
  start-page: 4759
  year: 2010
  ident: boe-7-11-4364-R20
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-09-2572
  contributor:
    fullname: Ostrander
– volume: 17
  start-page: 046010
  year: 2012
  ident: boe-7-11-4364-R44
  publication-title: J. Biomed. Opt.
  doi: 10.1117/1.JBO.17.4.046010
  contributor:
    fullname: Sepehr
– volume: 64
  start-page: 2054
  year: 2004
  ident: boe-7-11-4364-R41
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-03-3196
  contributor:
    fullname: Cairns
– volume: 285
  start-page: 9317
  year: 2010
  ident: boe-7-11-4364-R7
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.C110.104448
  contributor:
    fullname: Lu
– volume: 65
  start-page: 1180
  year: 2005
  ident: boe-7-11-4364-R17
  publication-title: Cancer Res.
  doi: 10.1158/0008-5472.CAN-04-3031
  contributor:
    fullname: Skala
– volume: 104
  start-page: 19494
  year: 2007
  ident: boe-7-11-4364-R18
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0708425104
  contributor:
    fullname: Skala
– volume: 17
  start-page: 671
  year: 2015
  ident: boe-7-11-4364-R28
  publication-title: Neoplasia
  doi: 10.1016/j.neo.2015.08.005
  contributor:
    fullname: Simões
– volume: 12
  start-page: R94
  year: 2010
  ident: boe-7-11-4364-R40
  publication-title: Breast Cancer Res.
  doi: 10.1186/bcr2773
  contributor:
    fullname: Louie
– volume: 34
  start-page: 2303
  year: 2016
  ident: boe-7-11-4364-R1
  publication-title: J. Clin. Oncol.
  doi: 10.1200/JCO.2015.65.8609
  contributor:
    fullname: Henry
– volume: 254
  start-page: 4764
  year: 1979
  ident: boe-7-11-4364-R12
  publication-title: J. Biol. Chem.
  doi: 10.1016/S0021-9258(17)30079-0
  contributor:
    fullname: Chance
– volume: 9
  start-page: e90746
  year: 2014
  ident: boe-7-11-4364-R23
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0090746
  contributor:
    fullname: Shah
– volume: 92
  start-page: 5510
  year: 1995
  ident: boe-7-11-4364-R36
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.92.12.5510
  contributor:
    fullname: Wang
– volume: 379
  start-page: 432
  year: 2012
  ident: boe-7-11-4364-R2
  publication-title: Lancet
  doi: 10.1016/S0140-6736(11)61625-5
  contributor:
    fullname: Peto
– volume: 16
  start-page: 992
  year: 2014
  ident: boe-7-11-4364-R9
  publication-title: Nat. Cell Biol.
  doi: 10.1038/ncb3039
  contributor:
    fullname: LeBleu
– volume: 73
  start-page: 636
  year: 2001
  ident: boe-7-11-4364-R16
  publication-title: Photochem. Photobiol.
  doi: 10.1562/0031-8655(2001)0730636AMOFCT2.0.CO2
  contributor:
    fullname: Drezek
– volume: 8
  start-page: 335
  year: 2001
  ident: boe-7-11-4364-R15
  publication-title: Opt. Express
  doi: 10.1364/OE.8.000335
  contributor:
    fullname: Ramanujam
– volume: 52
  start-page: 1399
  year: 1992
  ident: boe-7-11-4364-R26
  publication-title: Cancer Res.
  contributor:
    fullname: Aslakson
– volume: 21
  start-page: 060503
  year: 2016
  ident: boe-7-11-4364-R30
  publication-title: J. Biomed. Opt.
  doi: 10.1117/1.JBO.21.6.060503
  contributor:
    fullname: Hou
– volume: 6
  start-page: 559
  year: 2015
  ident: boe-7-11-4364-R32
  publication-title: Biomed. Opt. Express
  doi: 10.1364/BOE.6.000559
  contributor:
    fullname: Walsh
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Title Optical redox ratio identifies metastatic potential-dependent changes in breast cancer cell metabolism
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