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Review | Open Access

Molecular mechanisms of cellular metabolic homeostasis in stem cells

Xiaoyu Li1Ou Jiang1Songlin Wang1,2,3,4,5( )
Salivary Gland Disease Center and Beijing Key Laboratory of Tooth Regeneration and Function Reconstruction, Beijing Laboratory of Oral Health and Beijing Stomatological Hospital, Capital Medical University, Beijing, China
Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Capital Medical University, Beijing, China
Immunology Research Center for Oral and Systemic Health, Beijing Friendship Hospital, Capital Medical University, Beijing, China
Laboratory for Oral and General Health Integration and Translation, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
Research Unit of Tooth Development and Regeneration, Chinese Academy of Medical Sciences, Beijing, China
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Abstract

Many tissues and organ systems have intrinsic regeneration capabilities that are largely driven and maintained by tissue-resident stem cell populations. In recent years, growing evidence has demonstrated that cellular metabolic homeostasis plays a central role in mediating stem cell fate, tissue regeneration, and homeostasis. Thus, a thorough understanding of the mechanisms that regulate metabolic homeostasis in stem cells may contribute to our knowledge on how tissue homeostasis is maintained and provide novel insights for disease management. In this review, we summarize the known relationship between the regulation of metabolic homeostasis and molecular pathways in stem cells. We also discuss potential targets of metabolic homeostasis in disease therapy and describe the current limitations and future directions in the development of these novel therapeutic targets.

References

1

Folmes, C. D., Dzeja, P. P., Nelson, T. J. & Terzic, A. Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 11, 596–606 (2012).

2

Liu, K. et al. Cellular metabolism and homeostasis in pluripotency regulation. Protein Cell 11, 630–640 (2020).

3

Meacham, C. E., DeVilbiss, A. W. & Morrison, S. J. Metabolic regulation of somatic stem cells in vivo. Nat. Rev. Mol. Cell Biol. 23, 428–443 (2022).

4

Jin, Y. et al. Application of stem cells in regeneration medicine. MedComm 4, e291 (2023).

5

Seydel, C. Single-cell metabolomics hits its stride. Nat. Methods 18, 1452–1456 (2021).

6

Chandel, N. S. Carbohydrate metabolism. Cold Spring Harb. Perspect. Biol. 13, a040568 (2021).

7

Chandel, N. S., Jasper, H., Ho, T. T. & Passegué, E. Metabolic regulation of stem cell function in tissue homeostasis and organismal ageing. Nat. Cell Biol. 18, 823–832 (2016).

8

Cliff, T. S. et al. MYC controls human pluripotent stem cell fate decisions through regulation of metabolic flux. Cell Stem Cell 21, 502–516 e9 (2017).

9

Kikani, C. & Xiao, M. Glutamine metabolism co‐ordinates the cell‐cycle with cell fate in stem cells. FASEB J. 36, 629–642.e8 (2022).

10

Chapman, N. M., Boothby, M. R. & Chi, H. Metabolic coordination of T cell quiescence and activation. Nat. Rev. Immunol. 20, 55–70 (2020).

11

Pladevall-Morera, D. & Zylicz, J. J. Chromatin as a sensor of metabolic changes during early development. Front. Cell Dev. Biol. 10, 1014498 (2022).

12

Baksh, S. C. et al. Extracellular serine controls epidermal stem cell fate and tumour initiation. Nat. Cell Biol. 22, 779–790 (2020).

13

Samanta, D. & Semenza, G. L. Serine synthesis helps hypoxic cancer stem cells regulate redox. Cancer Res. 76, 6458–6462 (2016).

14

van Gastel, N. & Carmeliet, G. Metabolic regulation of skeletal cell fate and function in physiology and disease. Nat. Metab. 3, 11–20 (2021).

15

Ning, K. et al. Update on the effects of energy metabolism in bone marrow mesenchymal stem cells differentiation. Mol. Metab. 58, 101450 (2022).

16

Gu, W. et al. Glycolytic metabolism plays a functional role in regulating human pluripotent stem cell state. Cell Stem Cell 19, 476–490 (2016).

17

Liu, W. & Chen, G. Regulation of energy metabolism in human pluripotent stem cells. Cell Mol. Life Sci. 78, 8097–8108 (2021).

18

Nakamura-Ishizu, A., Ito, K. & Suda, T. Hematopoietic stem cell metabolism during development and aging. Dev. Cell 54, 239–255 (2020).

19

van Gastel, N. & Scadden, D. T. Young haematopoietic stem cells are picky eaters. Cell Res. 31, 377–378 (2021).

20

Chen, Z., Guo, Q., Song, G. & Hou, Y. Molecular regulation of hematopoietic stem cell quiescence. Cell Mol. Life Sci. 79, 218 (2022).

21

Ding, H. et al. Inhibiting aerobic glycolysis suppresses renal interstitial fibroblast activation and renal fibrosis. Am. J. Physiol. Ren. Physiol. 313, F561–F575 (2017).

22

Rodríguez-Colman, M. et al. Interplay between metabolic identities in the intestinal crypt supports stem cell function. Nature 543, 424–427 (2017).

23

Shyh-Chang, N., Daley, G. Q. & Cantley, L. C. Stem cell metabolism in tissue development and aging. Development 140, 2535–2547 (2013).

24

Pascale, R. M. et al. The Warburg effect 97 years after its discovery. Cancers 12, 2819 (2020).

25

Warburg, O. On respiratory impairment in cancer cells. Science 124, 269–270 (1956).

26

Flores, A. et al. Lactate dehydrogenase activity drives hair follicle stem cell activation. Nat. Cell Biol. 19, 1017–1026 (2017).

27

Bensard, C. L. et al. Regulation of tumor initiation by the mitochondrial pyruvate carrier. Cell Metab. 31, 284–300 e7 (2020).

28

Li, C. et al. Loss of sphingosine kinase 2 promotes the expansion of hematopoietic stem cells by improving their metabolic fitness. Blood 140, 1686–1701 (2022).

29

Wang, Z. et al. Enhanced glycolysis-mediated energy production in alveolar stem cells is required for alveolar regeneration. Cell Stem Cell 30, 1028–1042 e7 (2023).

30

Ryall, J. G. et al. The NAD(+)-dependent SIRT1 deacetylase translates a metabolic switch into regulatory epigenetics in skeletal muscle stem cells. Cell Stem Cell 16, 171–183 (2015).

31

Forte, D. et al. Bone marrow mesenchymal stem cells support acute myeloid leukemia bioenergetics and enhance antioxidant defense and escape from chemotherapy. Cell Metab. 32, 829–843 e9 (2020).

32

Yu, W. M. et al. Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell 12, 62–74 (2013).

33

Lin, C. et al. Impaired mitochondrial oxidative metabolism in skeletal progenitor cells leads to musculoskeletal disintegration. Nat. Commun. 13, 6869 (2022).

34

Pattappa, G., Heywood, H. K., de Bruijn, J. D. & Lee, D. A. The metabolism of human mesenchymal stem cells during proliferation and differentiation. J. Cell Physiol. 226, 2562–2570 (2011).

35

Huang, T. et al. Iron oxide nanoparticles augment the intercellular mitochondrial transfer-mediated therapy. Sci. Adv. 7, eabj0534 (2021).

36

Sivanand, S., Viney, I. & Wellen, K. E. Spatiotemporal control of acetyl-CoA metabolism in chromatin regulation. Trends Biochem. Sci. 43, 61–74 (2018).

37

Martinez-Reyes, I., Chandel, N. S. & Mitochondrial, T. C. A. cycle metabolites control physiology and disease. Nat. Commun. 11, 102 (2020).

38

Serefidou, M., Venkatasubramani, A. V. & Imhof, A. The impact of one carbon metabolism on histone methylation. Front Genet 10, 764 (2019).

39

Xie, N. et al. NAD(+) metabolism: pathophysiologic mechanisms and therapeutic potential. Signal Transduct. Target Ther. 5, 227 (2020).

40

Wang, H. et al. Nicotinamide mononucleotide supplementation improves mitochondrial dysfunction and rescues cellular senescence by NAD(+)/Sirt3 pathway in mesenchymal stem cells. Int. J. Mol. Sci. 23, 14739 (2022).

41

Pi, C. et al. Nicotinamide phosphoribosyltransferase postpones rat bone marrow mesenchymal stem cell senescence by mediating NAD(+)-Sirt1 signaling. Aging 11, 3505–3522 (2019).

42

Fang, J. et al. NAD+ salvage governs the immunosuppressive capacity of mesenchymal stem cells. Cell Mol. Immunol. 20, 1171–1185 (2023).

43

Gupta, S. & Santoro, R. Regulation and roles of the nucleolus in embryonic stem cells: from ribosome biogenesis to genome organization. Stem Cell Rep. 15, 1206–1219 (2020).

44

Li, W. et al. Nuclear localization of mitochondrial TCA cycle enzymes modulates pluripotency via histone acetylation. Nat. Commun. 13, 7414 (2022).

45

Yanes, O. et al. Metabolic oxidation regulates embryonic stem cell differentiation. Nat. Chem. Biol. 6, 411–417 (2010).

46

Clemot, M., Senos Demarco, R. & Jones, D. L. Lipid mediated regulation of adult stem cell behavior. Front. Cell Dev. Biol. 8, 115 (2020).

47

Wang, B., Wang, H., Li, Y. & Song, L. Lipid metabolism within the bone micro-environment is closely associated with bone metabolism in physiological and pathophysiological stages. Lipids Health Dis. 21, 5 (2022).

48

Kinder, M. et al. Hematopoietic stem cell function requires 12/15-lipoxygenase-dependent fatty acid metabolism. Blood 115, 5012–5022 (2010).

49

van Gastel, N. et al. Lipid availability determines fate of skeletal progenitor cells via SOX9. Nature 579, 111–117 (2020).

50

Hilgendorf, K. I. et al. Omega-3 fatty acids activate ciliary FFAR4 to control adipogenesis. Cell 179, 1289–1305 e21 (2019).

51

Bowers, M. et al. FASN-dependent lipid metabolism links neurogenic stem/progenitor cell activity to learning and memory deficits. Cell Stem Cell 27, 98–109 e11 (2020).

52

Madsen, S., Ramosaj, M. & Knobloch, M. Lipid metabolism in focus: how the build-up and breakdown of lipids affects stem cells. Development 148, dev191924 (2021).

53

Mistry, J. J. et al. Free fatty-acid transport via CD36 drives beta-oxidation-mediated hematopoietic stem cell response to infection. Nat. Commun. 12, 7130 (2021).

54

Yi, Y. et al. Fatty acid synthesis and oxidation regulate human endoderm differentiation by mediating SMAD3 nuclear localization via acetylation. Dev. Cell 58, 1670–1687 e4 (2023).

55

Mihaylova, M. M. et al. Fasting activates fatty acid oxidation to enhance intestinal stem cell function during homeostasis and aging. Cell Stem Cell 22, 769–778 e4 (2018).

56

Zheng, Z. et al. How high-fat diet affects bone in mice: a systematic review and meta-analysis. Obes. Rev. 20, e13493 (2022).

57

Luo, Y. et al. Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab. 22, 886–94 (2015).

58

Shahbodi, M., Emami, S. A., Javadi, B. & Tayarani-Najaran, Z. Effects of thymoquinone on adipocyte differentiation in human adipose-derived stem cells. Cell Biochem. Biophys. 80, 771–779 (2022).

59

Li, C. et al. Amino acid catabolism regulates hematopoietic stem cell proteostasis via a GCN2-eIF2alpha axis. Cell Stem Cell 29, 1119–1134 e7 (2022).

60

Liu, X. et al. PPM1K regulates hematopoiesis and leukemogenesis through CDC20-mediated ubiquitination of MEIS1 and p21. Cell Rep. 23, 1461–1475 (2018).

61

Zhang, F. et al. Excessive branched-chain amino acid accumulation restricts mesenchymal stem cell-based therapy efficacy in myocardial infarction. Signal Transduct. Target Ther. 7, 171 (2022).

62

Pavlova, N. N. et al. As extracellular glutamine levels decline, asparagine becomes an essential amino acid. Cell Metab. 27, 428–438 e5 (2018).

63

Kim, C. S. et al. Glutamine metabolism controls stem cell fate reversibility and long-term maintenance in the hair follicle. Cell Metab. 32, 629–642 e8 (2020).

64

Xu, M. et al. L-arginine homeostasis governs adult neural stem cell activation by modulating energy metabolism in vivo. EMBO J. 42, e112647 (2023).

65

Dai, Z., Ramesh, V. & Locasale, J. W. The evolving metabolic landscape of chromatin biology and epigenetics. Nat. Rev. Genet. 21, 737–753 (2020).

66

Steinberg, G. R. & Carling, D. AMP-activated protein kinase: the current landscape for drug development. Nat. Rev. Drug Discov. 18, 527–551 (2019).

67

Trefts, E. & Shaw, R. J. AMPK: restoring metabolic homeostasis over space and time. Mol. Cell 81, 3677–3690 (2021).

68

Yu, J. et al. Metabolic and proteostatic differences in quiescent and active neural stem cells. Neural Regen. Res. 19, 43–48 (2024).

69

Herzig, S. & Shaw, R. J. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat. Rev. Mol. Cell Biol. 19, 121–135 (2018).

70
Cheung, P. C. et al. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem J. 346, 659–669 (2000). Pt 3.
71

Thornton, C., Snowden, M. A. & Carling, D. Identification of a novel AMP-activated protein kinase beta subunit isoform that is highly expressed in skeletal muscle. J. Biol. Chem. 273, 12443–12450 (1998).

72

Stapleton, D. et al. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271, 611–614 (1996).

73

Crunkhorn, S. A new route to regulating AMPK activity. Nat. Rev. Drug Discov. 20, 175 (2021).

74

Steinberg, G. R. & Hardie, D. G. New insights into activation and function of the AMPK. Nat. Rev. Mol. Cell Biol. 24, 255–272 (2023).

75

Alessi, D. R., Sakamoto, K. & Bayascas, J. R. LKB1-dependent signaling pathways. Annu Rev. Biochem. 75, 137–163 (2006).

76

Marcelo, K. L., Means, A. R. & York, B. The Ca(2+)/calmodulin/CaMKK2 axis: nature’s metabolic CaMshaft. Trends Endocrinol. Metab. 27, 706–718 (2016).

77

Yako, H. et al. Role of pyruvate in maintaining cell viability and energy production under high-glucose conditions. Sci. Rep. 11, 18910 (2021).

78

Song, C. et al. Elevated exogenous pyruvate potentiates mesodermal differentiation through metabolic modulation and AMPK/mTOR pathway in human embryonic stem cells. Stem Cell Rep. 13, 338–351 (2019).

79

Ballhause, T. M. et al. Fracture healing in a mouse model of Hajdu-Cheney-Syndrome with high turnover osteopenia results in decreased biomechanical stability. Sci. Rep. 13, 11418 (2023).

80

Lee, S. Y. & Long, F. Notch signaling suppresses glucose metabolism in mesenchymal progenitors to restrict osteoblast differentiation. J. Clin. Investig. 128, 5573–5586 (2018).

81

Luo, J. Autophagy and ethanol neurotoxicity. Autophagy 10, 2099–2108 (2014).

82

Miao, Z. F. et al. A metformin-responsive metabolic pathway controls distinct steps in gastric progenitor fate decisions and maturation. Cell Stem Cell 26, 910–925 e6 (2020).

83

Zheng, J. et al. MSCs ameliorate hepatocellular apoptosis mediated by PINK1-dependent mitophagy in liver ischemia/reperfusion injury through AMPKalpha activation. Cell Death Dis. 11, 256 (2020).

84

Hardie, D. G., Schaffer, B. E. & Brunet, A. AMPK: an energy-sensing pathway with multiple inputs and outputs. Trends Cell Biol. 26, 190–201 (2016).

85
Kimura, T. & Nakano, T. Regulation of stem cell systems by PI3K/Akt signaling. In Regul Netw Stem Cells. (eds Rajasekhar, V. K. and Vemuri, M. C.) pp. 309–318 (2009).
86

He, Y. et al. Targeting PI3K/Akt signal transduction for cancer therapy. Signal Transduct. Target Ther. 6, 425 (2021).

87

Peng, Y. et al. Platelet rich plasma clot releasate preconditioning induced PI3K/AKT/NFkappaB signaling enhances survival and regenerative function of rat bone marrow mesenchymal stem cells in hostile microenvironments. Stem Cells Dev. 22, 3236–3251 (2013).

88

Cao, Z. et al. Hepatocyte growth factor (HGF) and stem cell factor (SCF) maintained the stemness of human bone marrow mesenchymal stem cells (hBMSCs) during long-term expansion by preserving mitochondrial function via the PI3K/AKT, ERK1/2, and STAT3 signaling pathways. Stem Cell Res. Ther. 11, 329 (2020).

89

Wang, Z. et al. Ginsenoside Rg1 prevents bone marrow mesenchymal stem cell senescence via NRF2 and PI3K/Akt signaling. Free Radic. Biol. Med. 174, 182–194 (2021).

90

Yang, Y. et al. Endogenous IGF signaling directs heterogeneous mesoderm differentiation in human embryonic stem cells. Cell Rep. 29, 3374–3384 e5 (2019).

91

Ren, Z. et al. Insulin promotes mitochondrial respiration and survival through PI3K/AKT/GSK3 pathway in human embryonic stem cells. Stem Cell Rep. 15, 1362–1376 (2020).

92

Tellechea, M. F., Chagraoui, J., Cohen, S. & Sauvageau, G. Towards clinically meaningful expansion of human HSCs. Cell Res. 33, 659–660 (2023).

93

Siegemund, S. et al. IP3 3-kinase B controls hematopoietic stem cell homeostasis and prevents lethal hematopoietic failure in mice. Blood 125, 2786–2797 (2015).

94

He, J. et al. MSC spheroids-loaded collagen hydrogels simultaneously promote neuronal differentiation and suppress inflammatory reaction through PI3K-Akt signaling pathway. Biomaterials 265, 120448 (2021).

95

Liu, G. Y. & Sabatini, D. M. mTOR at the nexus of nutrition, growth, ageing and disease. Nat. Rev. Mol. Cell Biol. 21, 183–203 (2020).

96

Goul, C., Peruzzo, R. & Zoncu, R. The molecular basis of nutrient sensing and signalling by mTORC1 in metabolism regulation and disease. Nat. Rev. Mol. Cell Biol. 24, 857–875 (2023).

97

Rousseau, A. & Bertolotti, A. Regulation of proteasome assembly and activity in health and disease. Nat. Rev. Mol. Cell Biol. 19, 697–712 (2018).

98

Sen, B. et al. mTORC2 regulates mechanically induced cytoskeletal reorganization and lineage selection in marrow-derived mesenchymal stem cells. J. Bone Min. Res. 29, 78–89 (2014).

99

Huang, T. et al. Aging reduces an ERRalpha-directed mitochondrial glutaminase expression suppressing glutamine anaplerosis and osteogenic differentiation of mesenchymal stem cells. Stem Cells 35, 411–424 (2017).

100

Zhao, S. et al. Engineering exosomes derived from subcutaneous fat MSCs specially promote cartilage repair as miR-199a-3p delivery vehicles in Osteoarthritis. J. Nanobiotechnol. 21, 341 (2023).

101

Xu, K. et al. Nesfatin-1 promotes the osteogenic differentiation of tendon-derived stem cells and the pathogenesis of heterotopic ossification in rat tendons via the mTOR pathway. Front. Cell Dev. Biol. 8, 547342 (2020).

102

Borsa, M. et al. Autophagy preserves hematopoietic stem cells by restraining MTORC1-mediated cellular anabolism. Autophagy 1–13 (2023).

103

Li, X. et al. Mechanisms and rejuvenation strategies for aged hematopoietic stem cells. J. Hematol. Oncol. 13, 31 (2020).

104

Chen, C., Liu, Y., Liu, Y. & Zheng, P. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci. Signal 2, ra75 (2009).

105

Haupt, R. et al. Enhancing the protection of influenza virus vaccines with BECC TLR4 adjuvant in aged mice. Sci. Rep. 13, 715 (2023).

106

Magee, J. A. et al. Temporal changes in PTEN and mTORC2 regulation of hematopoietic stem cell self-renewal and leukemia suppression. Cell Stem Cell 11, 415–428 (2012).

107

Xu, X. et al. The mTORC1-eIF4F axis controls paused pluripotency. EMBO Rep. 23, e53081 (2022).

108

Hu, Q. et al. JAK/STAT pathway: extracellular signals, diseases, immunity, and therapeutic regimens. Front. Bioeng. Biotechnol. 11, 1110765 (2023).

109

Morris, R., Kershaw, N. J. & Babon, J. J. The molecular details of cytokine signaling via the JAK/STAT pathway. Protein Sci. 27, 1984–2009 (2018).

110

Philips, R. L. et al. The JAK-STAT pathway at 30: Much learned, much more to do. Cell 185, 3857–3876 (2022).

111

Deng, W. et al. Hair follicle-derived mesenchymal stem cells decrease alopecia areata mouse hair loss and reduce inflammation around the hair follicle. Stem Cell Res. Ther. 12, 548 (2021).

112

Wang, T. et al. JAK/STAT3-regulated fatty acid beta-oxidation is critical for breast cancer stem cell self-renewal and chemoresistance. Cell Metab. 27, 136–150 e5 (2018).

113

Mantel, C. et al. Mouse hematopoietic cell-targeted STAT3 deletion: stem/progenitor cell defects, mitochondrial dysfunction, ROS overproduction, and a rapid aging-like phenotype. Blood 120, 2589–2599 (2012).

114

Herrera, S. C. & Bach, E. A. JAK/STAT signaling in stem cells and regeneration: from Drosophila to vertebrates. Development 146, dev167643 (2019).

115

Kong, R. et al. A feedforward loop between JAK/STAT downstream target p115 and STAT in germline stem cells. Stem Cell Rep. 18, 1940–1953 (2023).

116

Wang, L. et al. The study on the regulation of th cells by mesenchymal stem cells through the JAK-STAT signaling pathway to protect naturally aged sepsis model rats. Front. Immunol. 13, 820685 (2022).

117

Jitschin, R. et al. Inflammation-induced glycolytic switch controls suppressivity of mesenchymal stem cells via STAT1 glycosylation. Leukemia 33, 1783–1796 (2019).

118

Trelford, C. B., Dagnino, L. & Di Guglielmo, G. M. Transforming growth factor-β in tumour development. Front. Mol. Biosci. 9, 991612 (2022).

119

Fu, H. et al. A Nodal enhanced micropeptide NEMEP regulates glucose uptake during mesendoderm differentiation of embryonic stem cells. Nat. Commun. 13, 3984 (2022).

120

Li, Y. et al. IFT20 governs mesenchymal stem cell fate through positively regulating TGF-beta-Smad2/3-Glut1 signaling mediated glucose metabolism. Redox Biol. 54, 102373 (2022).

121

Gao, F. Y. et al. c-MYC mediates the crosstalk between breast cancer cells and tumor microenvironment. Cell Commun. Signal 21, 28 (2023).

122

Cai, C. et al. c-Myc regulates neural stem cell quiescence and activation by coordinating the cell cycle and mitochondrial remodeling. Signal Transduct. Target Ther. 6, 306 (2021).

123

Garcia-Prat, L. et al. TFEB-mediated endolysosomal activity controls human hematopoietic stem cell fate. Cell Stem Cell 28, 1838–1850 e10 (2021).

International Journal of Oral Science
Article number: 52
Cite this article:
Li X, Jiang O, Wang S. Molecular mechanisms of cellular metabolic homeostasis in stem cells. International Journal of Oral Science, 2023, 15: 52. https://doi.org/10.1038/s41368-023-00262-z

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Received: 02 November 2023
Revised: 12 November 2023
Accepted: 12 November 2023
Published: 01 December 2023
© The Author(s) 2023

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