Table 1.

Potential regulation of ribosome biogenesis in response to anabolic and catabolic stimuli.

Stimulus	Type	Characteristic	Model	Marker of ribosome biogenesis	References
Anabolic	Resistance exercise	12 sessions in 5 weeks, knee extension	Human	Tendency to increase in [total RNA]	(Haddad et al., 2005)
		Acute leg exercise (4 sets of 10 reps)	Human	Increase in S6K1 and RPS6 phosphorylation	(Glover et al., 2008a)
		3 sessions/week, 20 weeks. Microarray	Human	Down-regulation of 14 ribosomal protein genes associated with the mTOR-related expression network in the subjects with the highest muscle hypertrophy	(Phillips et al., 2013)
		Acute resistance exercise (arm)	Human	Increase in RPS6 phosphorylation, 45 pre-rRNA and c-myc mRNA expression	(Nader et al., 2014)
		Neural stimulation: twice a week for 6 weeks	Rat	Increase in S6K phosphorylation	(Baar and Esser, 1999)
		Neural stimulation: 2 bouts of 30min	Rat	Increase in [total RNA] and amount, in S6K1 phosphorylation	(Haddad and Adams, 2006)
	Resistance exercise + protein ingestion	Leg exercise combined with protein ingestion, 2 sessions/week, 21 weeks	Human	Increase in mTOR, S6K and RPS6 phosphorylation 1h after acute execise combined with protein ingestion	(Hulmi et al., 2009)
	Mechanical overload	Synergist ablation	Mouse	Increase in [total RNA], 47S pre-RNA expression, RNA Pol I regulon expression, c-myc expression, UBF expression	(von Walden et al., 2012)
			Mouse	Increase in [total RNA], S6K1 phosphorylation	(Miyazaki et al., 2011)
			Mouse	Increase in [total RNA], 28S + 18S content, S6K1 phosphorylation, UBF protein expression	(Goodman et al., 2011)
			Mouse	Activation of the Wnt/βcatenin/cmyc pathway	(Armstrong et al., 2006)
			Mouse	Increased [total RNA] associated with increased in c-myc expression	(Chaillou et al., 2013)
			Rat	Increase in [total RNA], S6K and RPS6 phosphorylation, total RPS6 protein expression	(Chaillou et al., 2012)
	Reloading after atrophy	Reloading after hindlimb suspension	Mouse	Increase in [total RNA] and total RNA content	(Dapp et al., 2004)
			Rat	Increase in [total RNA] and total RNA content	(Heinemeier et al., 2009)
	Serum stimulation	Myotubes treated with 20% FBS	L6 myotube	Increase in ribosomal RNA content	(Nader et al., 2005)
Catabolic	Aging	24 vs 70 years old- Acute resistance exercise	Human	No basal difference in S6K phosphorylation and protein synthesis. Increase in S6K phosphorylation and protein synthesis blunts in elderly after resistance exercise	(Kumar et al., 2009)
		27 vs 70 years old- Acute resistance exercise	Human	No increase in S6K1 and protein synthesis in aged patients after resistance exercise	(Fry et al., 2011)
		18–25 vs 60–75 years old- 12 weeks of resistance training combined with protein ingestion	Human	Increased phosphorylation of S6K after resistance training combined with protein ingestion is less pronounced in elderly	(Farnfield et al., 2012)
		6 vs 30 month old	Rat	Similar amount of total RNA per muscle	(Haddad and Adams, 2006)
	Cachexia	COPD	Human	Decrease in S6K phosphorylation in hypoxemic compared with non-hypoxemic COPD patients	(Favier et al., 2010)
		Critically ill	Human	Decrease in mTORC1 and S6K phosphorylation in critically ill patients compared to control subjects	(Constantin et al., 2011)
		Colorectal cancer	Mouse	Decrease in S6K phosphorylation in cancer mouse associated with skeletal muscle atrophy and reduced protein synthesis	(White et al., 2011)
		Glucocorticoid administration (dexamethasone)	Rat	Decrease in S6K phosphorylation and β-catenin protein expression	(Schakman et al., 2008)
		Chronic kidney disease	Rat	No changes in [total RNA] and S6K phosphorylation	(Chen et al., 2008)
		Atrophy induced by fasting, diabetes mellitus, renal failure and tumor implantation. Micro-array	Rat	Increase in RPL12 and nucleolin mRNA, two markers of ribosomal assembly	(Lecker et al., 2004)
	Disuse	Unilateral unloading	Human	Decrease in [total RNA]	(Haddad et al., 2005)
			Human	Decrease in [total RNA]	(Gamrin et al., 1998)
		Inactivity after abdominal surgery	Human	Decrease in [total RNA]	(Petersson et al., 1990)
		Hindlimb suspension and immobilization	Rat	Decrease in [total RNA]	(Babij and Booth, 1988)
		Hindlimb suspension	Rat	Decrease in [total RNA]	(Heinemeier et al., 2009)
	Denervation	Long-term spinal cord injury	Human	Decrease in [total RNA] in SCI subjects	(Bickel et al., 2003)
		Spinal cord injury	Rat	Decrease in total RNA concentration and content	(Haddad et al., 2003)
		Sciatic nerve transection	Rat	Up-regulation of several ribosomal proteins. Down-regulation of a few ribosomal proteins.	(Sun et al., 2012)
		Sciatic nerve transection	Mouse	Activation of mTORC1 in denervated muscle associated with increased expression of RPS6 and RPL7	(Quy et al., 2013)
		Sciatic nerve transection	Mouse	Activation of mTORC1 signaling and decrease in rRNA expression	(Machida et al., 2012)

[total RNA], total RNA concentration; COPD, chronic obstructive pulmonary disease; SCI, spinal cord injury.